the foxtail (setaria) species-group

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Invited Review The Foxtail (Setaria) Species-Group Jack Dekker, Weed Biology Laboratory, Agronomy Department, Iowa State University, Ames, IA 50011 USA; [email protected] Abstract. The weedy Setaria species (giant, green, yellow, knotroot and bristly foxtail) compose one of the worst weed groups interfering with world agriculture, and in other disturbed and managed habitats. These five weed species, together with their crop counterparts (foxtail millet, korali), form the foxtail species-group. Five successive waves of Setaria spp. invasion from pre-agricultural times to the present have resulted in widespread infestation of the disturbed, arable, temperate regions of the earth. These invasions have resulted in considerable economic and environmental costs. The success of the Setaria species-group is due to their intimate evolutionary relationship with humans, disturbance, agriculture and land management. The ability to rapidly adapt to local conditions is the hallmark of this weedy group. Genotypic and phenotypic biodiversity provide this species-group with traits that allow them to invade, colonize, adapt to, and endure in a wide range of habitats around the world. The phenotypic life history traits important to weedy Setaria spp. success begin with the induction of dormancy in seed during embryogenesis. The formation of long-lived, heterogeneous seed pools in the soil is the inevitable consequence of the dormant seed rain. In soil seed pools, after-ripening, the occurance and timing of seedling emergence, and the induction of secondary (summer) dormancy are regulated by seasonally and diurnally varying soil oxygen, water and temperature signals. Precise and variable timing of seedling emergence ensures Setaria a dominant place in disturbed and managed communities during the growth and reproductive phases that follow. Once established in a community, phenotypic plasticity inherent in an individual weedy Setaria sp. plant allow it to maximize its growth, form and reproduction to the specific local conditions it encounters, including competitive interactions with neighbors. Traits controlling the plastic development of plant architecture include the ability to form one or more tillering shoots whose stature and number are precisely sized to local conditions. A complex pattern of branching, from plant to spikelet, provides diverse microenvironments within which different levels of dormancy are induced in individual seeds on a panicle, and among panicles on a common plant. Traits for adaptation to stress in weedy Setaria spp. include tolerance to many inhibitory chemicals (e.g. herbicides, salt), mechanical damage and drought. Genetic traits such as self-pollenation and small genome size contribute to a highly diverse collection of locally adapted genotypes and phenotypes ready to exploit any opportunities provided by a cropping system. Self-pollenating Setaria spp. exist in wild, weed and crop variants, an ideal genetic condition ensuring both long- term stability and novelty. Weedy Setaria spp. populations have low to exceedingly low amounts of total genetic variation, unusually low intra-population genetic diversity, and unusually high genetic diversity between populations compared to an "average" plant species. These traits result spatially in local populations that are unusually homogeneous, typically consisting of a single multilocus genotype. Either a generally- or specifically-adapted genotype of an individual Setaria species might predominate in that local population. Across the landscape different single-genotype populations dominate particular local sites, providing novel genetics to the region via dispersal and gene flow when conditions change. Across North America, populations of S. viridis and S. geniculata are genetically differentiated along a north- 1

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Page 1: The Foxtail (Setaria) Species-Group

Invited Review

The Foxtail (Setaria) Species-Group

Jack Dekker, Weed Biology Laboratory, Agronomy Department, Iowa State University, Ames, IA 50011 USA; [email protected] Abstract. The weedy Setaria species (giant, green, yellow, knotroot and bristly foxtail) compose one of the worst weed groups interfering with world agriculture, and in other disturbed and managed habitats. These five weed species, together with their crop counterparts (foxtail millet, korali), form the foxtail species-group. Five successive waves of Setaria spp. invasion from pre-agricultural times to the present have resulted in widespread infestation of the disturbed, arable, temperate regions of the earth. These invasions have resulted in considerable economic and environmental costs. The success of the Setaria species-group is due to their intimate evolutionary relationship with humans, disturbance, agriculture and land management. The ability to rapidly adapt to local conditions is the hallmark of this weedy group. Genotypic and phenotypic biodiversity provide this species-group with traits that allow them to invade, colonize, adapt to, and endure in a wide range of habitats around the world. The phenotypic life history traits important to weedy Setaria spp. success begin with the induction of dormancy in seed during embryogenesis. The formation of long-lived, heterogeneous seed pools in the soil is the inevitable consequence of the dormant seed rain. In soil seed pools, after-ripening, the occurance and timing of seedling emergence, and the induction of secondary (summer) dormancy are regulated by seasonally and diurnally varying soil oxygen, water and temperature signals. Precise and variable timing of seedling emergence ensures Setaria a dominant place in disturbed and managed communities during the growth and reproductive phases that follow. Once established in a community, phenotypic plasticity inherent in an individual weedy Setaria sp. plant allow it to maximize its growth, form and reproduction to the specific local conditions it encounters, including competitive interactions with neighbors. Traits controlling the plastic development of plant architecture include the ability to form one or more tillering shoots whose stature and number are precisely sized to local conditions. A complex pattern of branching, from plant to spikelet, provides diverse microenvironments within which different levels of dormancy are induced in individual seeds on a panicle, and among panicles on a common plant. Traits for adaptation to stress in weedy Setaria spp. include tolerance to many inhibitory chemicals (e.g. herbicides, salt), mechanical damage and drought. Genetic traits such as self-pollenation and small genome size contribute to a highly diverse collection of locally adapted genotypes and phenotypes ready to exploit any opportunities provided by a cropping system. Self-pollenating Setaria spp. exist in wild, weed and crop variants, an ideal genetic condition ensuring both long-term stability and novelty. Weedy Setaria spp. populations have low to exceedingly low amounts of total genetic variation, unusually low intra-population genetic diversity, and unusually high genetic diversity between populations compared to an "average" plant species. These traits result spatially in local populations that are unusually homogeneous, typically consisting of a single multilocus genotype. Either a generally- or specifically-adapted genotype of an individual Setaria species might predominate in that local population. Across the landscape different single-genotype populations dominate particular local sites, providing novel genetics to the region via dispersal and gene flow when conditions change. Across North America, populations of S. viridis and S. geniculata are genetically differentiated along a north-

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south gradient. The past history of invasion and colonization, the successful life histories of locally adapted weedy Setaria spp., and the evolutionary potential of this weed group emphasize the need for accurate predictions of its behavior. Weedy Setaria spp. management is the mangement of local selection pressure and the consequential adaptation. Farmers, land managers, policy-makers and regulators, homeowners and consumers need accurate information about weedy Setaria spp. to predict and guide management decisions based on economics, risk and environmental sustainability. Nomeclature: green foxtail , Setaria viridis, subspecies viridis (L.) Beauv. SETVI; foxtail millet, Setaria viridis, subspecies italica) SETIT; yellow foxtail, Setaria glauca (Weigel) Hubb. SETLU; giant foxtail, S. faberii Herrm. SETFA; bristly foxtail, Setaria verticillata (L.) Beauv. SETVE; knotroot foxtail, S. geniculata SETGE

INTRODUCTION

The foxtails are members of the Setaria genus and are one of the worst weed groups interfering with North American and world agriculture and land management (Holm et al., 1977, 1979, 1997). The weedy Setaria spp. include S. viridis subspecies viridis (L.) Beauv. (green foxtail), S. glauca (Weigel) Hubb. (yellow foxtail), S. faberii Herrm. (giant foxtail), S. verticillata (L.) Beauv. (bristly foxtail), and S. geniculata (Lamarck) Beauv. (knotroot foxtail) (Pohl, 1951, 1966; Rominger, 1962). The genus Setaria also contains the crop foxtail millet (S. viridis subsp. italica) whose geographic distribution and evolutionary history is intimately connected with the weedy members of Setaria (de Wet, 1979, 1995).

Therefore, a review of the agricultural Setaria appropriately begins at the level of the Setaria species-group (a group of closely related species, usually with partially overlapping ranges; Lincoln et al., 1998), a wild-crop-weed complex (de Wet, 1966). Herein the term Setaria species-group (spp.-gp.) will be used when referring to properties shared by the five foxtail weed species and foxtail millet. Reviews of Setaria spp.-gp. have been published previously (S. glauca and S. verticillata, Steel et al., 1983; S. viridis, Douglas et al., 1985; Setaria spp.-gp., Dekker, 2003).

The success of the Setaria spp.-gp. is due to their intimate evolutionary relationship with humans, disturbance, agriculture, and land management. Genotypic and phenotypic biodiversity provide this species-group with traits that allow them to invade, colonize, adapt to and endure in a wide range of disturbed habitats in temperate, tropical, and sub-tropical regions.

Why have the weedy Setaria spp. spread globally over the last 5-9000 years? How did they get to be such a major weedy pest? What are the specific traits that allow them to dominate agricultural fields? Why is Setaria still a dominant species-group in North American agriculture after continuous use of highly effective herbicides for almost 50 years? What will the Setaria species-group do in the future? What do we know, not know, and need to know to manage them? The answer to these questions begins with the history of global invasion of the Setaria spp.-gp. Subsequent success of the foxtails is revealed by their local adaptation. The consequences of this local adaptation and evolution are apparent in its life history. The conclusions implied by Setaria spp.-gp. invasion, local adaptation and life history could advise future management systems.

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HISTORY OF GLOBAL INVASION

`There appears to be five major phases, or waves, of wild-weed-crop Setaria spp.

invasion in earth's history. The origin of the genus and the original wild Eurasian Setaria sp. was probably Africa, based on the large number of Setaria spp. from there (74 of 125), as well as genomic evidence of tropical origins (Lakshmi and Ranjekar, 1984; Prasado Rao, 1987; Rominger, 1962; Simpson, 1990; Stapf and Hubbard, 1930). The tropical genus Setaria dispersed to Eurasia and adapted to a wider range of environmental conditions and habitats. In the second phase, a S. viridis weedy progenitor species spread over Eurasia as a wild colonizing species. The wild, progenitor Setaria spp. that invaded Eurasia in many locations after leaving its African home was most likely a diploid annual similar to S. viridis, subsp. viridis (Kihara and Kishimoto, 1942; Koernicke and Werner, 1885a, b; Li, 1934; Li et al., 1942, 1945; Prasado Rao et al., 1987; Rominger, 1962; Simpson, 1990; Werth, 1937; Willweber-Kishimoto, 1962). Speciation and adaptation followed this spread in geographic distribution to subtropical, and then temperate, regions. Parallel to this, with possibly more ancient antecedants, S. glauca arose and spread throughout China. With domestication, both S. viridis and S. glauca then spread as a weed and a crop (foxtail millet and korali). Foxtail millet was a crop in China 6000 years B.P. (Before Present) (Cheng, 1973; Li and Wu, 1996; Naeiri and Belliard, 1987), while its use as a crop in Europe dates to 3600 B.P. (Dembinska, 1976; Helbaek, 1960; Neuweiler, 1946; de Wet and Harlan, 1975). Setaria glauca seed were gathered from wild plants and later cultivated in India (de Wet et al., 1979; de Wet, 1992). Other weedy Setaria species arose from S. viridis-like ancestors (Khosla and Sharma, 1973), including polyploid specialists such as S. verticillata, S. verticillata and S. faberii. In the third wave, weedy Setaria spp. spread to the New World at two different times: pre-Columbian (before ca. 1500 A.D.) and post-Columbian invasions (after ca. 1500 A.D.). The pre-Columbian origins of S. geniculata, the only weedy Setaria native to the New World, suggest an ancient dispersal event eastward from the Eurasia to the Americas (Rominger, 1962). A species of Setaria, probably S. geniculata, was the oldest cultivated cereal in the Americas, its origins dating to almost 9000 B.P. (Callen, 1965, 1967; de Wet, 1992; Smith, 1968). Prehistoric migration of Setaria could date from when the ancestors of contemporary native Americans first crossed the Bering Straits land bridge connecting Asia and North America (Beringia; approximately 10 to 20,000 B.P.). The S. glauca invasion of the Americas came primarily from Asia (Wang et al., 1995b). The post-Columbian dispersal of weedy Setaria by Eurasian human emigration over the last 500 years is most likely the major source of the weedy Setaria spp. introductions we see in North American agroecosystems today. Setaria spp. have expanded their range since their introduction to North America in the last several hundred years as a consequence of global trade and human-mediated dispersal. The fourth wave occurred recently by an extremely rare allo(tetra)polyploidization event giving rise to a fertile hybridization product in southern China, S. faberii (Wang et al., 1995b). Setaria faberii was first introduced to North America in the 1920's near New York City (Warwick, 1990). Soon thereafter it was found in Philadelphia (1931) and Missouri (1932). Since that time S. faberii spread rapidly in the eastern and midwestern states. In the post-WWII era, S. faberii spread explosively across the North American maize and cereal growing regions (Slife, 1954). The introduction and adoption of the herbicide 2,4-D to control dicotyledonous weeds created an opportunity for, and population shift to, grassy weeds like the Setaria (Alex,

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1972; Blackshaw et al., 1981a; Dexter et al., 1981; Manthey and Nalawaja, 1987; Oliver and Schreiber, 1971; Pohl, 1951; Schreiber, 1977; Vanden Born, 1971; Warwick, 1990). Introduction of other new selective herbicides, as well as expansion of maize and soybean production in North America, accelerated these trends. More recently, S. faberii has spread northward into Ontario in the 1970's. Since the turn of the millenium S. faberii has appeared for the first time in the Red River valley of North Dakota with the very recent introduction of soybean culture (G. Kegode, personal communication). In little over a half century, S. faberii has invaded and colonized large parts of the most fertile, disturbed areas of North America. Currently we are experiencing a fifth invasive phase, from the late 1970's through the 2000's, with the appearance of many new herbicide resistant biotypes of Setaria (Holt and LeBaron, 1990; Reschly et al., 1996; Ritter, et al., 1989; Santelmann and Meade, 1961; Stoltenberg and Wiederholt, 1995; Tranel and Dekker, 1996, 2002; Thornhill and Dekker, 1993; Volenberg et al., 2001; Wiederholt and Stoltenberg, 1996). Concurrent with this is the ongoing incremental spread of S. faberii and S. glauca in the northern prairies of North America.

Geographic invasion can also be viewed as genetic invasion: Setaria polyploidization. Four polyploid Setaria spp. (S. geniculata, S. glauca, S. verticillata and S. faberii) have invaded, and are adapted to, specific niches. They all exist in a narrower geographic distribution than the diploid S. viridis.

LOCAL ADAPTATION

The consequence of this long history of global invasion is the current genotypic composition of locally-adapted Setaria species. The spatial structure of these locally-adapted genotypes is apparent in their present-day biogeography and population genetic structure. The locally-adapted phenotypes that reside within this spatial structure are the consequence of intentional (domestication) and unintentional (weedy) selection pressures in human-managed habitats. TAXONOMY AND GENOTYPIC VARIATION

World-wide there are 125 Setaria species divided among several subgenera, 74 of these species are from Africa (Hubbard, 1915; Rominger, 1962). The taxonomy of the genus is very complex, and an accurate classification has been confounded by the high degree of overlapping morphological characters both within and between species, and the diverse polyploidy levels within the genus. The genus Setaria belongs to the tribe Paniceae, subfamily Panicoideae and family Poaceae (Pohl, 1978). S. faberii, S. glauca, S. verticillata, S. viridis (both subspp. italica and viridis) are Eurasian adventives. The origins of S. geniculata are of particular note. S. geniculata, a perennial, is the only weedy Setaria native to the New World, and very closely resembles S. glauca, an annual species of Eurasian origin (Rominger, 1962; Wang et al., 1995b). Setaria geniculata and S. glauca are frequently misidentified by weed managers. It has been suggested that the cause of this enigma was an ancient, pre-Columbian, dispersal event westward from the Old to New World (Rominger, 1962). Foxtail millet (S. viridis subsp. italica) and weedy S. viridis subsp. viridis are subspecies of S. viridis and have continuous and overlapping genetic variation, evidence of the weedy origins of the crop (Prasada Rao et al., 1986; Wang et al., 1995a).

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A number of morphological variants of Setaria viridis have been named (e.g. S. viridis var. major (Gaud.) Posp., giant green; S. viridis var. robusta-alba Schreiber, robust white; S. viridis var. robusta-purpurea Schreiber, robust purple; S. viridis var. pachystachys (Franch et Savat.) Makino et Nemoto; S. viridis, var. vivipara (Bertol.) Parl.; Dore and McNeill, 1980; Hubbard, 1915; Kawano and Miyaki, 1983; Schreiber and Oliver, 1971)), although their taxonomic validity has been questioned (Wang et al., 1995a). Often the most striking morphological differences among Setaria arise from biotypes with similar allelic variation (e.g. compare S. viridis subsp. viridis var. pachystachys and S. viridis subsp. italica race maxima), while genotypic variation can be wide within nearly identical morphologies (e.g. compare Old World S. glauca and New World S. geniculata). Many of the morphological variants described as biotypes are in fact extreme examples of continuous characters (e.g. leaf coloration in S. viridis var. robusta-purpurea); Schreiber and Oliver, 1971). POPULATION GENETIC STRUCTURE

Population genetic structure of locally-adapted foxtail genotypes forms the basis of present-day plant spatial and temporal organization, and has practical implications for weed management (Barrett and Husband, 1990). Genetic Diversity in Weedy Setaria Spp.

The pattern of genetic diversity within an individual weedy Setaria sp. is characterized by unusually low intra-population genetic diversity, and unusually high genetic diversity between populations, compared to an "average" plant (Hamrick and Godt, 1990) (Wang et al., 1995a, 1995b). These two patterns of population genetic structure appear to typify introduced, self-pollinated weeds that are able to rapidly adapt to local conditions after invasion and colonization (e.g. Brown and Marshall, 1981; Rice and Jain, 1985; Barrett and Richardson, 1986; Barrett, 1988; Barrett and Shore, 1989). In comparison to an "average" plant species, weedy Setaria species contain low to exceedingly low amounts of total genetic variation (Hamrick and Godt, 1990; Wang et al., 1995a, 199b). Although relative genetic diversity within each of the several Setaria species is very low, differences between homogeneous populations are high, indicating a strong tendency for local adaptation by a single genotype. Nearly all populations consist of a single multilocus genotype. Apomixis in the Setaria cannot be ruled out (Emery, 1957). Genetic Pattern of Colonization and Regional Differentiation

In addition to the potential selective forces responsible for low genetic diversity and high population differentiation, stochastic forces have played a major role in shaping Setaria population genetic structure. Perhaps the most important phenomenon, in this respect, has been a history of genetic bottlenecks (a sudden decrease in population density with a corresponding reduction of total genetic variability; Lincoln et al., 1998) associated with founder events (a small fraction of the genetic variation of a parent population or species is present in the small number of founder members of a new colony or population; Lincoln et al., 1998), genetic drift (occurrence of random changes in the gene frequencies of small isolated populations, not due to selection, mutation or immigration; Lincoln et al., 1998), and natural selection (Wang et al., 1995a, 1995b). The founder effect has been observed in S. viridis to a certain degree. S. viridis accessions from North America have reduced allelic richness compared to those of Eurasia. Genetic drift probably has occurred in S. viridis, as indicated by the many fixed alleles in North American accessions. Multiple introductions of S. viridis, in the absence of local adaptation, should have produced a random, mosaic pattern of geographic distribution among North American accessions. Instead, a strong intra-continental differentiation is observed in S. viridis

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populations, both in Eurasia and North America (Jusef and Pernes, 1985; Wang et al., 1995a). S. viridis populations in North America are genetically differentiated into northern and southern groups separated on either side of a line at about 43.5° N latitude. The northern type is less variable than southern type. This regional divergence suggests that natural selection has partitioned S. viridis along a north-south gradient. These observations imply that the present patterning among S. viridis populations in North America is the consequence of multiple introductions into the New World followed by local adaptation and regional differentiation.

Setaria glauca populations are genetically clustered into overlapping Asian, European, and North American groups (Wang et al., 1995b). S. glauca populations from the native range (Eurasia) contain greater genetic diversity and a higher number of unique alleles than those from the introduced range (North America). Within Eurasia, Asian populations have greater genetic diversity than those from Europe, indicating S. glauca originated in Asia, not Europe. These observations indicate there have been numerous introductions of S. glauca from Eurasia to North America, the majority from Asia. This pattern may also explain the enigma of the origins of S. glauca and S. geniculata. The pattern of S. glauca genetic variability is North American was unexpected: nearly the entire diversity of this species appears to be encompassed by accessions from Iowa, whereas populations collected from other North American locations were nearly monomorphic for the same multilocus genotype (Wang et al., 1995b). In this respect, it is significant or coincidental that this pattern was repeated in the diversity data for S. viridis, also a native of Eurasia (Wang et al., 1995a). Iowa possesses a surprising Setaria genetic diversity: all five weedy Setaria species are present. Typically two or more Setaria species occur in the same field at the same time. Iowa is the center of the north-south agro-ecological gradient in North America, perhaps leading to greater environmental heterogeneity.

Despite originating on different continents, the genetic diversity patterns for S. geniculata parallel those for S. glauca and S. viridis: greater genetic diversity occurs in accessions from the New World compared to those from the introduced range (Eurasia) (Wang et al., 1995b). This most likely reflects genetic bottlenecks associated with sampling a limited number of founding propagules and the history of multiple introductions from the Americas to Eurasia. The population genetic structure of S. geniculata consists of three nearly distinct clusters, groups from Eurasia, northern United States, southern United States. Accessions from Eurasia and North America are approximately equally diverse genetically. Within North America, S. geniculata accessions were strongly differentiated into southern and northern groups at about the Kansas-Oklahoma border (37° N latitude); indicating greater genetic differentiation within North American populations than between North American and Eurasian populations.

S. faberii contains virtually no allozyme variation. Fifty of the 51 accessions surveyed by Wang et al., (1995b) were fixed for the same multilocus genotype. Genetic Variation and Evolutionary Success of Colonizers

The population genetic structure of many widely distributed, introduced, self-pollinating, weed species clearly indicates that a high level of genetic variation is not a prerequisite for successful colonization and evolutionary success (Allard, 1965; Barrett and Shore, 1989). Two contrasting, adaptive strategies are hypothesized to explain weedy adaptation and the success of colonizers: genetic polymorphism with the development of locally adapted genotypes ("specialists"), and phenotypic plasticity for the development of "general purpose" genotypes (generalists) adaptable to a wide range of environmental conditions (Baker, 1965, 1974; Bradshaw, 1965; Barrett and Richardson, 1986).

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Weedy Setaria population genetic structure allows some insight into the dichotomy of generalism versus specialization. Setaria possess both generalists and specific strategy types. A key observation is that although a single, multilocus genotype predominates or is fixed in all populations, not all multilocus genotypes are equally prevalent within individual weedy Setaria species (Wang et al., 1995a, 1995b). The most striking example of this is in S. glauca, where the most common multilocus genotype was found in 53 (of 94 evaluated) accessions surveyed by Wang et al., (1995b) from widely separated geographic areas in Europe, Asia, and North America. Overlaying this pattern of homogeneity were other, less abundant S. glauca genotypes, each with a more narrow geographical and ecological distribution.

The population genetic structure of S. viridis suggests that this species also possesses both generally adapted and specially adapted genotypes. Many S. viridis populations are genetically strongly differentiated (e. g., northern and southern North America), while other populations remain identical. The most widely distributed S. viridis genotype (fixed multilocus genotype) occurred in 25 (of 168 evaluated) accessions from six countries, from both the Old World and the New World (Wang et al., 1995a, 1995b). Interestingly, this common genotype has not yet been found in Iowa, despite the diversity of S. viridis populations found in this state.

These observations reveal a complex hedge-betting strategy by individual weedy Setaria species that balances general adaptation with the additional niche opportunities available with specialization. The ratio of general to special genotypes in locally adapted populations in a species for invasion is quite different within S. glauca, S. geniculata and S. viridis (Wang et al., 1995a, 1995b). BIOGEOGRAPHY AND PHENOTYPIC VARIATION

The geographic distribution of locally adapted Setaria genotypes, and the phenotypic adaptation due to selection imposed by human agricultural activities, provide information about the current biogeography of Setaria. Geographical Distribution The genus Setaria is cosmopolitan, and can be found on every landmass in the world except the polar regions (Prasada Rao et al., 1986; Rominger, 1962). In the western hemisphere, Setaria has its center of distribution in Brazil, and radiates poleward north and south (Rominger, 1962). The weedy Setaria spp. are primarily temperate species but are widely distributed between 45° S and 55° N latitudes (Holm et al., 1977, 1997; Wang et al., 1995a, b). They are found in every state in the continental U.S. and every province in Canada (Lorenzi and Jeffery, 1987). The Eurasian Setaria are rare in the southwest U.S., Mexico and more southerly, tropical regions. Locally Adapted Phenotypes

One of the most striking observations of Setaria behavior is the occurrence of phenotypic heterogeneity, rather than genetic diversity, among the individuals of a population as a means of exploiting a locality (Scheiner, 1993; Wang et al., 1995a, 1995b). This phenotypic heterogeneity takes the form of phenotypic plasticity and somatic polymorphism in many of its most important traits, especially during reproduction. Most of the phenotype variation of Setaria has not been characterized. Only the most obvious behaviors and morphologies have been described, those characters most apparent in management situations.

A rapid increase in herbicide resistant Setaria variants has been observed in the last 25 years. The resistance mechanisms include those that exclude, as well as metabolically degrade, the herbicides (e.g. Thornhill and Dekker, 1993; Wang and Dekker, 1995). Physiological

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variation in dormancy and germinability exists (Dekker et al., 1996; Norris and Schoner, 1980). Variation in drought tolerance among the Setaria has been observed (Blackshaw et al., 1981a; Manthey and Nalewaja, 1982, 1987; Taylorson, 1986). Potentially salt-tolerant genotypes of S. viridis, var. pachystachys have been observed along the seacoasts of Japan (Chapman, 1992b; Kawano and Miyaki, 1983; author's personal observation, 1992 and 2000, data not reported). There may exist an intimate physiological and morphological relationship between drought tolerance, salt tolerance and seed dormancy. This is most apparent in extreme habitats where foxtail millet remains an important crop and cultivated cereal (e.g. Central Asia including Afghanistan, India, sub-Saharan Africa). Weed Population Shifts

Most changes in Setaria populations are difficult to experimentally document. The most obvious and dramatic Setaria population change in the last few decades has been the shift to herbicide resistant biotypes. Anecdotally, many weed managers have observed increased weed problems later in the season with the use herbicides since the late 1940's. Setaria population shifts in seedling emergence timing have been observed by Atchison (2001), including the shift to later emergence in the season. Seedling emergence of a cohort entering the soil at the same autumn time tended to occur later in the season as it aged from 1 to 3 years. In the third year the largest emergence occurred after layby (julian week 22-26) and control tactics ceased, compared to the first year when emergence was greatest early (julian week 14-21). Changes in tillage practices in the late 20th century provided selection pressure for changes in the location and soil depth from which Setaria seeds germinate and emerge (Buhler, 1995; Mester and Buhler, 1986; Yennish et al., 1992). Species Niche Differentiation

The geographic distribution of the Setaria has been expanding in North America in terms of species present, new habitats, and population density in occupied areas (Alex, 1972; Blackshaw et al., 1981a; Dexter et al., 1981; Manthey and Nalawaja, 1987; Oliver and Schreiber, 1971; Pohl, 1951; Schreiber, 1977; Vanden Born, 1971; Warwick, 1990). For example, in the Canadian prairies differential responses to soil moisture and temperature may be the cause of S. viridis and S. glauca spread and geographic distribution. S. viridis seed germination occurs faster and is better adapted to low moisture and high or extreme temperature regimes, than S. glauca (Blackshaw et al., 1981a; Manthey and Nalawaja, 1987). S. faberii can dominate S. glauca when grown together, but in less fertile conditions S. glauca can dominate and displace S. faberii by means of greater root growth when nitrogen availability is low (Schreiber, 1977; Schreiber and Orwick, 1978). S. verticillata vegetative growth is sensitive to shade, which may make it less competitive in cropping situations (Lee and Cavers, 1981). Changes in cropping practices and herbicide usage have been responsible for S. faberii invasion and spread northward from midwestern U.S. since 1960 (Warwick, 1990). Domestication

The Setaria species-group is one of the most ancient wild-weed-crop complexes in agriculture. Wild colonizing Setaria species adapted to pre-agricultural disturbances were first domesticated by gathering seeds from natural stands. Later, these seeds were sown purposefully and harvested.

The principal Setaria domesticate is S. viridis, subspecies italica (foxtail millet), but S. glauca (korali) has also been domesticated (Wang et al., 1995a; de Wet et al., 1979). Continuous hybridization among foxtail millet and Setaria has resulted in a wide variety of types with overlapping morphology and genetic constitution. S. viridis var. major (Gaudin) Pospichal

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(giant green foxtail) is believed to be a hybridization product of foxtail millet and S. viridis (Pohl, 1951, 1966; Rominger, 1962).

Foxtail millet possesses three different morphological land races based on plant and panicle morphology: races moharia, maxima and indica (Prasada Rao, 1987; de Wet et al., 1979). An alternative organization based on molecular evidence is provided by Fukunaga et al. (2002), who characterize Eurasian foxtail millet landraces into 5 geographic groups. Korali, domesticated S. glauca is an endemic kharif crop grown in India (Bor, 1960; de Wet et al., 1979). These ancient crop domestication events occurred independently in many different Eurasian locations (de Wet et al., 1979; Fukunaga et al., 1997; Jusuf and Pernes, 1985; Nguyen Van and Pernes, 1985; Prasado Rao et al., 1987). The most diversity is found within Chinese populations, possibly the first Eurasian location for foxtail millet domestication, although it most likely had multiple origins (Harlan, 1975).

Setaria domestication surprisingly appears to have occurred first in the Americas (9000 B.P.). Foxtail millet, S. viridis, subsp. italica, was domesticated as long ago as 6000 years B.P. in China and other Eurasia locations, making it one of the oldest cultivated cereals of Eurasia (Chang, 1973; Cheng, 1973; Gao and Cheng, 1988; Ho, 1969, 1975; Kawase and Sakamoto, 1984; Li and Wu, 1996; Naeiri and Belliard, 1987; Nai, 1963; Wheeler, 1950). These dates suggest early colonization by Setaria to the Americas from Asia over the Bering Strait land bridge at that time, a suggestion that might explain the genetic similarity enigma of S. glauca and S. geniculata (Rominger, 1962).

Intentionally and unintentionally, weedy and domestication traits have been exchanged by wild, weedy and crop variants of the same species in production fields since agriculture began, forming wild-weed-crop complexes (Darmency et al., 1987b; Harlan, 1965; Harlan et al., 1973). Hybridization and gene flow between wild, weedy and crop Setaria spp. in the same fields has occurred since the first wild relatives were affected by human agricultural activities. The partial reproductive isolating barriers between crop and weed variants becomes a positive advantage for weedy success when a new variant acquires weedy traits and invades the human-managed habitat (e.g. S. viridis, var. major; Darmency et al., 1987b). Human selection accelerates these phenotypic and adaptive changes in the crop, while disruptive selection maintains variant type unity in the wild-weed-crop complex (Prasado Rao et al., 1987).

At present, foxtail millet is a minor world crop. Several species of Setaria are still extensively collected as wild cereals (Bor, 1960; Bulmer, 1964; Chevalier, 1913, 1932; Dalziel, 1937; Monsalud et al., 1966). Foxtail millet (S. viridis) is prepared as human food in many ways, as well as being used as animal feed (Barrau, 1958; de Wet et al., 1979; Kadkol and Swaminathan, 1965; Monsalud et al., 1966; Rozhevitz and Shiskhin, 1934). It is not traded on world markets, but is in local markets. Setaria millets have not been the focus of modern plant breeding, crop improvement, biotechnology or international trade.

LIFE HISTORY

Successful assembly of Setaria spp. in local communities with other species is determined by key traits typifying their annual life history. The first assembly step in many agricultural fields is the emergence of seedlings or herbaceous foliage of perennial species. Successful foxtail seedlings then interact with other species in the locality. The competitive phase concludes with reproduction and entry of new seed into the soil.

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SOIL SEED POOLS AND SEEDLING EMERGENCE

Seedling emergence is the birth of a Setaria plant, its entrance into a local community, the first committed step in assembly with neighbors. Soil seed pool spatial structure, seed dormancy, and environment determine where and when seedlings emerge. Seedling emergence prediction guides early season risk management and the use of weed tactics. Time of seedling emergence is the single most important factor determining subsequent yield losses from, and competitiveness of, a weed. A weed's competitive success determines yield losses, seed bank replenishment and future weed infestations. Seed Dormancy and Soil Seed Pool Formation

One of the most important traits weedy Setaria spp. possess for invasiveness, colonizing ability and enduring occupation of a locality is their ability to form long-lived soil seed pools, the source of all future annual weed infestations (Buhler et al., 1997a; Dekker, 1999). Dormancy inherent in Setaria seeds inevitably leads to formation of soil seed pools. Significant heterogeneity in dormancy states among weedy Setaria seeds results in precisely timed germination over large temporal scales (hours to decades; Atchison, 2001; Dekker et al., 1996; Forcella et al., 1992, 1997). Soil seed pools consisting of a diverse collection of Setaria species, genotypes and dormancy phenotypes reveals a hedge-betting strategy for adaptation to changing conditions within agroecosystems (e.g. Cohen, 1966; Philippi and Seger, 1989). Heteroblasty. Individual Setaria panicles on a single parent plant produce a diverse array of seeds, each with potentially different dormancy states (heteroblasty) (Atchison, 2001; Dekker et al., 1996; Moore and Fletchall, 1963; Haar, 1998; Kollman, 1970; Martin, 1943; Nieto-Hatem, 1963; Schreiber, 1965a; Stanway, 1971; Taylorson, 1986; Vanden Born, 1971). Heterogeneity in dormancy states among seeds shed by a single plant allow them to subsequently emerge at appropriate times within a cropping season and in different years (Dekker et al., 1996; Forcella et al., 1997). Morphological variants of S. viridis (robust white, robust purple and giant green) have been reported indicating they do not possess seed dormancy (Schreiber, 1977). Triazine resistant S. faberii seed were reported to be inherently more dormant than susceptible biotypes (Tranel and Dekker, 1996, 2002), consistent with observations in other species (Mapplebeck et al., 1982). Vivipary (premature germination) in S. viridis plants have been observed (Dore and McNeill, 1980; Haar, 1998; Hubbard, 1915). Seed longevity in the soil. The length of time that weedy Setaria spp. seeds are able to survival in the soil is quite variable, but mortality decreases with depth of burial. The maximum period of survival in the soil varies by species: S. glauca: typical, 13 years; maximum, 30 years (Darlington; 1951; Dawson and Bruns, 1975; Kivilaan and Bandurski, 1973; Toole and Brown, 1946); S. viridis: maximum 10 to 39 years (Burnside et al.; 1981; Dawson and Bruns, 1975; Thomas et al., 1986; Toole and Brown, 1946); S. verticillata: maximum, 39 years (Toole and Brown, 1946). More typically, the majority of weedy Setaria spp. seed live in the soil for much shorter time periods (Atchison, 2001). In general, S. viridis and S. glauca seed on the surface lose viability sooner than buried seed (Banting et. al., 1973; Thomas et al., 1986). The rate of survival of Setaria seed is longer under uncultivated conditions (Stoller and Wax, 1974; Waldron, 1904). Burial of weedy Setaria spp. seed increases both the level of dormancy, viability, and the longevity, of those seeds, possibly due to decreased oxygen at greater depths or within soil aggregates (Banting et. al., 1973; Dekker and Hargrove, 2002; James, 1968; Pareja and Staniforth, 1985; Pareja et al., 1985; Stoller and Wax, 1974). Dawson and Bruns (1975) showed precipitation had no effect on S. viridis seed longevity in the soil.

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Regulation of Weedy Setaria spp. Seed Behavior The wide geographic range of adaptation, heterogeneity in dormancy phenotypes, and

genotypic diversity raise the question of what mechanisms in weedy Setaria spp. seeds drive seed behaviors (e.g., induction of dormancy, after-ripening, germination, induction of summer dormancy, and seedling emergence). There is evidence that soil water, temperature and oxygen play a unifying role in regulating both the global biogeographic distribution of weedy Setaria spp., as well as the responses of individual seeds in a soil microsite (Dekker, 2000; Dekker and Hargrove, 2002; Dekker et al., 2001).

The morphology of weedy Setaria spp. seeds provides clues about which environmental factors limit germination and maintain dormancy. The weedy Setaria spp. seed symplast (embryo, endosperm, and aleurone layer) is enveloped by several layers controlling its behavior, notably the hull (lemma, palea) and the caryopsis coat (Dekker et al., 1996; Rost, 1971, 1972, 1973, 1975; Rost and Lersten, 1973). The caryopsis coat is water- and gastight, and continuous except at the narrow placental pore opening on the basal end of the seed. The mature weedy Setaria spp. seed is capable of freely imbibing water and dissolved gases, but entry is restricted and regulated by the placental pore tissues, notably membrane control by the transfer aleurone cell layer (TACL; Rost and Lersten, 1970).

This morphology strongly suggests that seed germination is restricted by water availability in the soil, and by the amount of oxygen dissolved in water reaching the inside of the seed symplast to fuel metabolism. Oxygen solubility in the water entering the symplast is an inverse function of the diurnally, seasonally, and annually changing soil temperature. The control by this oxygen-limited, gas-tight morphology is supported by observations of increased germination when Setaria seed envelopes, including the caryopsis coat, are punctured (Dekker, et al., 1996; Stanway, 1971), as well as by the stimulatory effects of oxygen and carbon monoxide (Dekker and Hargrove, 2002).

Individual Setaria seed behavior appears to be regulated by the amount of oxygen dissolved in water taken into the seed over time. When adequate amounts of water and oxygen reach the embryo, sufficient energetic equivalents are generated to support germination metabolism (Bewley and Black, 1994). When inadequate amounts of oxygen reach the embryo, dormancy is maintained or secondary dormancy is induced (Corbineau and Côme, 1995). Given that Setaria seed behavior is regulated by the amount of oxygen dissolved in water taken into the seed over time, the signal stimulating Setaria behavior in an individual seed is oxygen mass per water volume of symplast (caryopsis) per time (e.g. hour, day): mass O2

volume H20-1 time-1

seed-1 (oxy-hydro time; Dekker et al., 2001). Germination and Seedling Emergence Dormancy, germination and environment. The inherent weedy Setaria spp. seed dormancy state responds to the immediate soil environment it encounters after abscission and dispersal, which determines its subsequent behavior (germination, seedling emergence, mortality or extended life in the soil). The influence of environmental factors on seeds in the soil changes with time. Light. The influence of light on weedy Setaria spp.a seed germinability is equivocal and, at best, small. Some report light has no effect on germination (Nakamura, 1962; Taylorson, 1982, 1986), others conclude light promotes germination (Povalitis, 1956; Holm and Miller, 1972). Emergence from depth in the soil indirectly supports a positive (Dawson and Bruns, 1962) and negative (Waldron, 1904) influence of light on weedy Setaria spp.seed germination. This variability may indicate an environmentally conditional response to light.

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Temperature. The influence of temperature on weedy Setaria spp. seed dormancy changes with time and development. Often the same temperatures can have opposite effects on seeds depending on their dormancy state. The range of temperatures stimulating weedy Setaria spp. seed germination widens with after-ripening, as more individuals become highly germinable (Norris and Schoner; 1980).

Low temperature (e.g. 5 C) and adequate moisture (stratification) is one of the most effective and consistent ways to after-ripen dormant weedy Setaria spp. seed (Anderson, 1968; Atchison, 2001; Dekker et al., 1996; Nieto-Hatem, 1963; Povalitis, 1956; Stanway, 1971; Vanden Born, 1971). Once fully after-ripened these same low temperatures can enforce dormancy in the same seed until temperatures capable of supporting the germination process are attained (i.e. 10 to 15 C or more). The duration (days to weeks) of stratification necessary to overcome dormancy is a function of the amount and variability of dormancy in the weedy Setaria spp. population (Atchison, 2001). After-ripening occurs under dry conditions, but with considerably longer time periods than when moist (e.g. more than a year) (Povalitis, 1956; Stanway, 1971; Thornhill, 1997; Vanden Born; 1971). Very low temperature (e.g. -20 to -50° C) and aerobic conditions can slow after-ripening almost entirely, yet retain seed viability (Dekker, personal observation, data not reported).

Temperatures of 20 to 25 C can rapidly promote germination of non-dormant and near-complete after-ripened seeds, but dormant seeds at those temperatures after-ripen very slowly or not at all. Optimal temperatures for weedy Setaria spp. seed germination are a function of the amount and heterogeneity of dormancy states among seed evaluated. As such, there is no single optima for any naturally occurring group of weedy Setaria spp. seed. Optimal weedy Setaria spp. seed germination temperatures have been reported, although few have characterized the extent or variability in dormancy among individuals of the population tested (e.g. Atchison, 2001): S. viridis, 15 to 35 C; S. glauca 20 to 25 C; S. verticillata, 25 to 40 C (Banting et al., 1973; Blackshaw et al., 1981a; Vanden Born 1971; Martin, 1943; Lauer, 1953; King, 1952; Norris and Schoner, 1980; Manthey and Nalawaja, 1987).

High temperatures (e.g. 30 C or greater) can either stimulate non-dormant seed to germinate or induce secondary (summer) dormancy. In other situations these high temperatures can speed after-ripening and release from dormancy, possibly due to heat damage and cracking of gas-tight weedy Setaria spp. seed envelopes (Taylorson and Brown, 1977). "Accelerated after-ripening" occurred in S. viridis, S. glauca and S. faberii by exposing seeds to 50 C for up to 14 days. High temperatures and moisture can induce secondary dormancy in mature, highly germinable, after-ripened S. faberii seed (Atchison, 2001; Taylorson, 1982, 1986), or have no affect on dormancy (Vanden Born 1971).

Diurnal temperature fluctuations increase germination of weedy Setaria spp. seeds when compared to germination in static temperature conditions (Anderson, 1968; James, 1968; Sells, 1965). Maximal weedy Setaria spp. seed germination occurred with daily alternating temperatures between about 20 and 35C, compared to other alternating temperature or constant temperature regimes (King, 1952). Moisture. weedy Setaria spp. seed germination requires adequate moisture, but exhibits a high level of tolerance to variable soil moisture conditions (Manthey and Nalawaja, 1987; King, 1952; Taylorson, 1986). Several types of moisture stress can both stimulate germination or induce dormancy (King, 1952; Taylorson, 1986). Temperature and moisture may have an interactive effect on the germination of S. viridis: soil moisture has a greater effect than temperature on S.

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viridis germination, but as water potential decreases the effect of temperature becomes greater (Blackshaw et al., 1981a). Gases. The gaseous components of agricultural soils influencing weedy Setaria spp. seed behavior include oxygen, nitrogen, carbon dioxide, water vapor and volatile metabolites such as carbon monoxide and ethylene (James, 1968; Siegel et al., 1962; Siegel and Siegel, 1987; Corbineau and Côme, 1995). The structural characteristics of the soil (texture, drainage, aggregation, crusting, and cracking) affect the gaseous environment within which Setaria seeds germinate (Pareja and Staniforth, 1985; Pareja, Staniforth, and Pareja, 1985).

Oxygen is required for germination of Setaria, and both oxygen and carbon monoxide affect Setaria seed behavior in the soil. S. faberii seed germination is markedly affected by O2 at levels above and below that of air (20% O2) (Dekker and Hargrove, 2002). The largest increase in germination occurs at O2 concentrations immediately greater than that of air. Carbon monoxide stimulated S. faberii germination at low (0.1-1.0%), but was inhibitory at high (75%), concentrations in air. These separate effects of CO occur in different physiological systems of dormant seeds at the same time: inhibition of mitochondrial respiration and an as yet uncharacterized physiological factor in the seed (Dekker and Hargrove, 2002). Disrupting Setaria seed envelopes and bypassing natural gas-tight barriers increases germination (Dekker et. al., 1996; Heise, 1941; Nieto-Hatem, 1963; Kollman, 1970; Peters and Yokum, 1961; Rost, 1975; Stanway, 1971; Taylorson and Brown, 1977). Periodicity of seedling emergence. In general, weedy Setaria spp. seeds are capable of germinating and emerging anytime the soil is unfrozen. Most Setaria seedlings emerge in the early part of the growing season of a locality (e.g. April-June in the northern hemisphere; Atchison, 2001; Buhler et al., 1997b; Forcella et al., 1992, 1997): S. viridis (Banting et al., 1973; Chepil, 1946; Dawson and Bruns; 1962); S. glauca (Dawson and Bruns, 1962, 1975; Manthey and Nalewaja,1987; Martin, 1943; Sells, 1965; Steel et al., 1983; Stoller and Wax, 1974); S. verticillata (Martin, 1943). With knowledge of dormancy states and environmental O2-H20 signals in a local seed pool it may be possible to predict Setaria emergence in a locality with precision (Dekker et al., 2001). Depth of seed germination from the soil. Weedy Setaria spp. seedlings emerge from relatively shallow depths in the soil, usually between 1 to 5 cm depth. Emergence is greatest at 1.5 to 2.5 cm and declines with depth to a maximum of about 7.5 to 14 cm (Buhler, 1995; Buhler and Mester, 1991; Dawson and Bruns, 1962; Gregg, 1973; Waldron, 1904). Emergence of weedy Setaria spp. does not usually occur on the soil surface except in the debris of no-till systems, an indication that light may not play an important role in seed germination. The soil depths from which the maximum S. faberii emergence occurs is a function of the tillage system, the greater the depth of tillage the deeper and more varied the seed placement and seedling emergence: 0 to 2 cm (no-till); 1 to 3 cm (disk); 1 to 4 cm (chisel plow); 1 to 5 cm (moldboard plow) (Mester and Buhler, 1986; Yenish et al. 1992). Atchison (2001) observed that S. faberii in the first year after dispersal emerged from shallower depths (0 to 5 vs. 5 to 10 cm), but emergence of older, more dormant seed was similar from these two depths. Others have correlated depth of emergence and seed weight, surmising that greater seed weight indicates more seed reserves (Dawson and Bruns; 1962; King, 1952). Oxygen content decreases with soil depth, inhibiting after-ripening and germination at greater depths and enforcing dormancy (Dekker and Hargrove, 2002; James, 1968). GROWTH AND DEVELOPMENT

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Once a seedling is successfully established, interactions with neighbors and the immediate environment determines whether a weedy Setaria plant becomes part of the extant community. Abiotic and biotic environmental constraints remove species that lack specific traits allowing them to compete with neighbors, utilize local resources effectively, and reproduce. In many agroecosystems weedy Setaria spp. are not the first species to emerge (Buhler et al., 1997b). In communities where it does emerge it often dominates other species, even those emerging earlier. Apparently, weedy Setaria spp. possess traits allowing them to more efficiently utilize resources and exclude neighbors. This may be evidence that weedy Setaria are keystone species (a species having a major influence upon community structure often in excess of that expected from its relative abundance; Lincoln et al., 1998) in disturbed communities. Other keystone weed species exist, species whose presence dominates community assembly of other species, but whom themselves are affected to a much lesser extent by competing species. This dominating role of weedy Setaria spp. is exacerbated when more than one Setaria species is present in a field. Removal of the more numerous Setaria species may allow other Setaria species to increase. The stability of Setaria in communities is a function of those competitive traits it possesses, or those of its neighbors, and is not due to biodiversity per se (e.g. species richeness, allele richness) (May, 1973). Somatic Plasticity

The ability of weedy Setaria spp. to compete efficiently at the expense of neighbors for resources is due to traits allowing highly efficient, plastic, growth (Pigliucci, 2001). The size and fecundity of any individual Setaria plant is a plastic growth response to the environmental conditions (light, water, gases, nutrients, temperature) and neighbors it encounters after it emerges from the soil (Pigliucci, 2001). Individual weedy Setaria seedlings have many physiological mechanisms, most of which have not been characterized, that result in precise and efficient sizing to their immediate environment (resources, deficits, inhibitors and neighbors). These plastic responses to environment can result in large differences in plant stature and fitness. Physiological traits that confer these abilities include those relating to nutrient acquisition, photosynthesis and plant architecture. The consequences of weedy Setaria spp. plasticity is most apparent in the size and extent of tillering of an individual plant. Primary (1°) tillers often branch when resources are available forming secondary (2°) and tertiary (3°) tillers from which fruiting panicles arise. For example, long day length photoperiods, little competition from neighbors, early seedling emergence and full season growth, ample nutrients and water, in full sunlight, can result in large S. faberii plants attaining 2 m height with multiple tillers and panicles, producing thousands of seeds. At the other extreme, a small S. viridis plant will result from a seedling emerging at the very end of the season, when the light portion of the photoperiod is very short, attaining the untillered height of 5 cm, with 2-3 leaves, producing a single panicle with one seed. Growth and environment. The weedy Setaria spp.are very competitive in cropping fields (e.g. Blackshaw et al., 1981b; Dryden and Whitehead, 1963; Harrison et al., 1985; Morrison et al., 1981; Rahman and Ashford, 1972; Staniforth, 1965). Changes in the plant community and resource availability associated with crop rotations, and changes in crop rotation, can affect the competitive ability of weedy Setaria (e.g. Alex et al., 1972; Dunham et al., 1958; Laudien and Koch, 1972; Schreiber, 1965b). Resource competition in agroecosystems by Setaria includes that for light, soil nutrients and pH, water and temperature

Weedy Setaria spp. plant size decreases with decreases in light and competitive shading by neighbors (e.g. Bubar and Morrison, 1984; Santlemann et al., 1963; VandenBorn, 1971). The

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changing photoperiod during the growing season also has important effects on growth and development, especially in combination with acquisition of growth requisites (Orwick and Schreiber, 1975; Schreiber and Orwick, 1978; VandenBorn, 1971). Setaria culms elongate in response to light competition. Setaria have C4 leaf-structural type of photosynthetic metabolism (Black et al., 1969; Elmore and Paul, 1983; Hattersley and Watson, 1992; Ku et al., 1974). Despite possessing this type of compensatory metabolism, photosynthesis in water-stressed S. faberii plants was enhanced with enriched carbon dioxide atmospheres (Sionit and Patterson, 1985).

Although triazine resistant biotypes (R) of many species have been shown to have reduced seed yield relative to susceptible variants (LeBaron and Gressel, 1982), it is not clear this reduction in growth and yield occurs in R biotypes of S. viridis (Ricroch et al., 1987). Pleiotropic effects resulting from the dynamic reorganization of a plant with the mutant psbA chloroplast gene in R biotypes may provide a competitive advantage in some stressful conditions (Dekker, 1993; Dekker and Sharkey, 1992; Tranel and Dekker, 2002).

Nutrient availabilty, soil fertility and soil pH affect the size of Setaria plants and their growth and competitive ability with other plants of a community (intra- and inter-specific competition) (e.g. Chambers and Holm, 1965; Hume, 1982; Kuzin, 1973; Moyer and Dryden, 1977; Moyer et al., 1979; Orwick and Schreiber, 1979; Schreiber and Orwick, 1978; Weaver and Hamill, 1985). Different Setaria species frequently co-habit the same field, exploiting overlapping niches in the available nutrient resources of a particular production system. The Setaria species that dominates can vary depending on the conditions of the locality.

Setaria plant size decreases (tiller and leaf number, height, shoot and root biomass) with decreasing available water (e.g. Alex et al., 1972; Nadeau, 1983; Nadeau and Morrison, 1983; Orwick and Schreiber, 1975). Water stress reduces photosynthetic rates in S. faberii (Sionit and Patterson, 1985). Setaria growth and development is dependent on temperature (e.g. Schreiber, 1965a). Mortality. Setaria plant mortality from density-dependent (e.g. effects of neighbors) and density-independent (e.g. predation, parasitism, catastrophe) causes is an important source of weed population losses (Douglas et al., 1985; Harper, 1977; Steele et al., 1983). Weedy Setaria spp. mortality, and its various sources, is poorly understood. REPRODUCTION AND THE SEED RAIN The life of an individual weedy Setaria parental plant ends with reproduction and the seed rain. In general, the larger the biomass of a Setaria plant, the more reproductive tillers it has, the more numerous its progeny. The first outwardly visible evidence of reproduction is the emergence of the panicle from the subtending leaf sheath. Reproduction ends with the abscission of dormant seed from the parent plant, the seed rain replenishing the soil seed pool. Fertilization

The pattern of flowering and seed fertilization is a complex process occurring on several different spatial and temporal scales: within and among individual panicles on the same plant, during the annual growing season, and during a daily or diurnal period. Pattern of flowering in the panicle. Panicles usually emerge after the summer solstice, and flowering commences and continues after that time into the autumn. There is considerable variation in the patterns of panicle tiller emergence, flowering, embryogenesis and seed abscission among and within weedy Setaria spp. inflorescences. Time of seedling emergence, as well as the photoperiod and temperature coinciding with an individual plant's seasonal growth

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period, are major determinants of these flowering phenomena (Haar, 1998; Stevens, 1960). The flowering pattern in S. faberii along the panicle has been described (Dekker et al., 1996): starting near (but not at) the distal end and proceeding in both the distal and basal direction. Pattern of seasonal flowering. The time from planting to the appearance of the first S. faberii and S. viridis panicle is highly variable and is dependent on the diurnal photoperiod (Nieto-Hatem, 1963; Schreiber and Oliver, 1971; Schreiber, 1965a; Stevens, 1960). Setaria appear to initiate flowering and fertilization in response to the shortening photoperiod (lengthening dark period) after the summer solstice. Long daylengths appear to prolong these reproductive responses, while continuous light markedly delays panicle production and inhibits flowering, in all the weedy and crop Setaria spp. (Fabian, 1938; King, 1952; Peters and Yokum, 1961; Peters et al., 1963; Santelman et al., 1963; Schreiber, 1965a; Vanden Born, 1971). Triazine resistant biotypes of S. viridis flower earlier than susceptible variants (Ricroch et al., 1987). Blooming in wild type biotypes is negatively correlated with temperature and positively with relative humidity (Li et al., 1935). The response of flowering to photoperiod in weedy Setaria spp. may be hastened by higher temperatures (Ricroch et al., 1987; Schreiber and Oliver, 1971). Pattern of diurnal flowering. Setaria flowering usually occurs during specific time periods of the day, depending on local environmental conditions, and is an endogenously regulated rhythm with two daily maxima peaks (i.e. 0400 to 0800 h and 1900 to 0000 h) in the dark (Li, 1935; Rangaswami Ayyangar et al, 1933; Willweber-Kishimoto, 1962). The average time between flower opening and closing is 70 min. (Kishimoto, 1938). Hybridization The weedy Setaria are primarily a self-pollenated species (Mulligan and Findlay, 1970; Pohl, 1951). Wind pollenation (anemophily) is the mode in those rare circumstances of outcrossing (Pohl, 1951; Nguyen Van and Pernes, 1985). Pollen and gene flow in the weedy Setaria can be intra-specific (autogamy, self-fertilization; allogamy, outcrossing) or inter-specific hybridization (introgression between different Setaria species).

Natural outcrossing between Setaria plants of the same species, intraspecific hybridization, does occur and is an important source of new variants. In S. viridis, spontaneous outcrossing rates among plants in the field have been observed to be between 0 and 7.6% of the autogamous rates (Darmency et al., 1987a; Prasado Rao et al., 1987; Till-Bottraud, 1992; Takashi and Hoshino, 1934; Li, 1934; Li et al., 1935; Macvicar and Parnell, 1941).

Introgression of pollen between weedy species, interspecific hybridization, is a rare event. When it does occur it can have very important consequences, although the progeny are almost always sterile (Clayton, 1980; Li et al.,1942; Osada, 1989; Poirier-Hamon and Pernes, 1986; Stace,1975; Till-Bottraud et al., 1992; Willweber-Kishimoto, 1962). Asexual Reproduction

Asexual (meiotic) reproduction is not a common mode of reproduction in weedy Setaria, and is probably limited to S. geniculata, a perennial species with short, branched, knotty rhizomes (Rominger, 1962). Agamospermy (seed formation without fertilization) in S. viridis has been noted (Mulligan and Findlay, 1970), and has also been suggested for S. glauca and S. verticillata (Steel et al., 1983). Apomixis has also been reported in other Setaria species within the Setaria subgenus (S. leucopila, S. machrostachya and S. texana; Chapman, 1992a; Emery, 1957). Setaria faberii and S. glauca tillers readily root in soil when cut, separated from the plant, and buried in moist soil, an important trait allowing weedy Setaria to reestablish themselves after cultivation and mowing (Barrau, 1958; Santlemann et al., 1963; Schreiber, 1965b)

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Speciation and Reproductive Barriers Between Setaria Species New Setaria species can be formed by several processes (e.g. mutation, hybridization,

polyploidization, etc.), but such events are very rare. Partial reproductive barriers exist between the Setaria species, a genetic condition favoring introgression and gene flow at very low levels within the species-group and wild-crop-weed complex (Darmency et al., 1987; de Wet, 1966; Harlan, 1965; Harlan et al., 1973). Panicle height differences, and times of fertilization (pollen shed; stigma receptivity), both prevent hybridization events from occurring between many populations (Willweber-Kishimoto, 1962). Reproductive barriers between the Setaria species does not occur at the level of pollen germination and pollen tube growth in the stigma in any combination of pollen and stigma among S. italica, S. viridis, S. faberii, S. glauca, and S. pallide-fusca (Willweber-Kishimoto, 1962). Polyploidization (either alloploidy or autoploidy) has played an active role in speciation and delimiting taxa in Setaria (Khosla and Sharma, 1973). Polyploidization of the more diverse and ancient S. viridis may have been the genesis of the specialized and less diverse Setaria spp. set (S. faberii, S. glauca, S. verticillata and S. geniculata). Allotetraploid forms of S. faberii and S. glauca have been explained as ancient crosses of S. viridis with an unknown diploid species (Li, 1942; Kholsa and Singh, 1971; Till-Bottraud et al., 1992). This polyploidization in S. faberii may be a relatively recent evolutionary event (Wang et al., 1995b). S. verticillata (n=18) may be the product of chromosome doubling of S. viridis, autotetraploidy (Till-Bottraud et al., 1992). Geographical barriers to inter-species hybridization in current times are much less important now than in the past. Genetics Molecular genetics. DNA of S. viridis subsp. italica has several distinguishing features: low nuclear DNA content (haploid, C-value, 1C: 0.82 pg), low proportion of repetitive DNA (30%), and the presence of a high melting point component (4.7-6.7% of the genome) (Lakshmi and Ranjekar, 1984; SivaRaman et al., 1986). The total proportion of repetitive DNA was the lowest value in the Poaceae family at the time it was reported (Lakshmi and Ranjekar, 1984). The authors suggest that the high melting component has a functional role in genomic adaptations to specific environments (e.g. dry, nutrient poor, high light). It has been suggested this high thermal stability in foxtail millet may indicate very little to no base sequence mismatch, a rare observation, or that this stability maintains internal homogeneity by 'cross over' fixation (Smith, 1976). A major part of the foxtail millet genome (85%) consists only of long interspersed repeated DNA sequences (greater than 1.5 kilo base pairs; SivaRaman et al., 1986). These long sequences can maintain genome size by slow rates of turnover, in which repeated DNA sequences are not subjected to mutations, deletions or base substitutions at a very rapid rate (Flavell, 1980; SivaRaman et al., 1986). The significance of genome size in phylogeny is not understood, the so-called 'C-value paradox' (Orgel and Crick, 1980). Cavalier-Smith (1978) asserts there is a good correlation between low C-values and strong r-selection for weedy qualities. Dawkins (1999) suggests that intragenomic selection pressure may lead to a decrease or elimination of "junk" DNA (untranslated introns) and therefore smaller genome size in colonizing, invasive species like Setaria. Cytogenetics. The typical nuclear genome of Setaria spp. has a complement of 9 chromosomes in its monoploid form (gametophytic egg, pollen; n=9=x). Sporophytic tissue within the genus includes the polyploid series of 2x (S. viridis, subsp. italica and viridis), 4x (S. faberii, S. glauca, S. geniculata, S. verticillata), 6x (S. verticillata), 8x (S. glauca, S. geniculata) possibilities. Genetic maps of foxtail millet have been constructed based on RFLP markers (Wang et al., 1998; Devos et al., 1998). Cytological evidence emphasizes the primacy of S. viridis, subsp. viridis as

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the progenitor species of all Eurasian Setaria weeds and crops (Li, 1942). The two genomic components that have contributed chromosome complements to the Setaria spp. include his "A" and "B genoms". S. viridis, subsp. viridis was the source of the "A genom" in the many Setaria spp., while the source of his "B genom" is unknown. Plant Architecture

The branching architecture of Setaria plants consists of hierarchically organized, nested, structural sets: tiller culm, panicle, fascicle, spikelet and floret, as in most grasses. Setaria spp. lant architecture is plastic, and includes the ability to form one or more tillering shoots whose stature and number are precisely sized to local conditions. A complex pattern of branching, from plant to spikelet, provides diverse microenvironments within which different levels of dormancy are induced in individual seeds of the panicle, and among panicles on a common plant.

The first externally visible event in the reproductive phase is the emergence of the immature panicle from the subtending leaf sheath of its tiller. Once flowering has proceeded basipetally to the bottom of the panicle the culm elongates and extends out of the leaf collar. This axis elongation is one of two means by which the light microenvironment in the panicle changes during flowering, fertilization and embryogenesis. A second developmental mechanism altering an individual spikelet microenvironment involves fascicle spacing in the inflorescence. These two mechanisms altering the light microenvironment of seeds may play a role in environmental control of dormancy induction (Dekker et al., 1996).

The inflorescence in the subgenus Setaria is usually narrow, terminal on the culm, very dense, cylindrical, and spicate, with very short branches (fascicles) only a few mm long (Rominger, 1962; Willweber-Kishimoto, 1962; Naryaswami, 1956). The fascicles are spirally arranged around the main axis, each bearing a number of branchlets.

The fascicle, the panicle branch, consists of 1 to six or more spikelets amid a cluster of setae (bristles) in a complicated system of branching (Naryaswami, 1956; Rominger, 1962). Spikelets are clustered on the rachis that diverges from the main panicle axis. The number of fertile spikets per fascicle within each S. faberii or S. viridis panicle is variable (e.g. 1 to 3), and plastic in response to environmental conditions (Clark and Pohl, 1996). Setaria glauca fascicles, unlike that of S. viridis or S. faberii, bear only a single spikelet. In the mature inflorescence, the number of fascicles per unit length of panicle axis decreases from the distal to the basal end (Dekker et al., 1996). This arrangement of fascicles is a second mechanism allowing greater light penetration to basal flowers of the panicle.

The basic unit of the Setaria inflorescence is a dorsally compressed, two-flowered spikelet disarticulating below the glumes and subtended by one to several bristle-like setae (Hitchcock, 1971; Rominger, 1962). The spikelet consists of the rachilla, a sterile or staminate floret below, a perfect floret above, and three empty glumes (Li et al., 1935; Willweber-Kishimoto, 1962). For S. viridis, S. faberii and S. verticillata the lower floret is entirely degenerated. In S. glauca the lower floret has no pistil, instead it has three well developed anthers which open 3 to 7 days after the upper floret (Willweber-Kishimoto, 1962). The perfect or fertile floret above is often referred to as the fruit, grain or seed. This seed is composed of an indurate, usually transversely wrinkled, lemma and palea (hull) of similar marking and texture, which tightly enclose the caryopsis within at maturity. The degree of rugosity of the lemma is a valuable taxonomic diagnostic character. Rugosity varies from smooth and shiny in foxtail millet, to finely ridged in S. viridis, to very coarse rugose seed in other Setaria species (Rominger, 1962). This rugosity may play a role in soil-seed contact (water, gas exchange) and seed germination. Setaria spikelets are subtended by one to several setae (stalks of abortive

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spikelets) that persist after the spikelets disperse (Chase, 1937; Hofmeister, 1868; Prasada Rao et al., 1986). It is these distinctive setae that give the inflorescence of Setaria spp. it characteristic appearance (foxtails). Embryogenesis

Embryogenesis in Setaria begins with anthesis and fertilization of the new embryo, and ends when the embryo, enveloped with parental tissues (i.e. lemma, palea, caryopsis coat), becomes physiologically separated from the parent plant (abscission). Formation of the seed. Three nuclear genomes cooperate and interact to form the Setaria seed or floret: zygote (2n), endosperm (3n) and the parent (2-8n). The parent contributes sporophytic tissues to the seed that both nurture and protect the developing embryo, as well as provide significant contributions to dormancy and control of post-abscission germination timing (e.g. seed envelopes such as the caryopsis coat), and physical protection in the soil. The duration of embryogenesis in an individual S. faberii seed grown in controlled environmental conditions is 8 to 15 days (Haar, 1998; Dekker et al., 1996). Induction of dormancy. The production of seeds with different germination requirements (dormancy) is a function of genotype, plant architecture and the environmental conditions during their life cycle. Earlier fertilized seeds on any Setaria panicle are relatively more dormant than those developing later (Haar,1998). Seed produced on 1° panicles (typically August in the Midwest U.S.) is more dormant than seed produced on 2° pancicles (September), which are in turn more dormant than seed on 3° panicles (October) (Haar,1998; Atchison (2001). Others have observed that decreasing temperature and photoperiod length result in increased dormancy in seeds (Schrieber, 1965a; Simpson, 1990).

Atchison (2001) observed that seed maturing early in the growing season in partial shade are considerably more dormant than those on nearby plants in full sun. Axis elongation and fascicle spacing are two mechanisms differentially modifying the light microenvironment of individual spikelets (Dekker et al., 1996). This differential light reception may be a mechanism by which different levels of dormancy are induced in individual florets of a panicle: relatively greater light levels are associated with relatively reduced dormancy in later maturing seeds on a panicle. Greater light penetration is correlated with relatively less dormancy in the more widely spaced basal florets, while the greater height and light above the soil surface (and competitors) is correlated with less dormant florets maturing later on an individual panicle (Atchison, 2001; Dekker et al., 1996; Haar, 1998).

Setaria faberii plants subjected to mowing produced seed with relatively more dormancy the later the main culm was cut, regardless of plant age or emergence time (Schreiber, 1965b). Fawcett and Slife (1978) observed that weedy Setaria plants treated with 2,4-D produced seed with less dormancy compared to an untreated control. Seed Abscission and Dispersal

Weedy Setaria spp. seeds become physiologically independent when the abscission layer in the pedicel forms, indicated by the red coloration of the placental pad on the caryopsis (Dekker et al., 1996). Abscission is a singular, threshold event in the life history of a new Setaria plant, but it is only a partial separation of the new and parental generations: parental, apoplastic tissues surround the seed symplast, affecting its ability to germinate.

Weedy Setaria spp. seeds separate (shatter) from the parent plant soon after abscission, but the time of dispersal varies based on pedicel deterioriation and wind. Seeds of the crop foxtail millet have been selected to resist shattering, allowing near complete harvest by the grower. Setaria seed dispersal occurs by gravity, animal (e.g. birds), wind, water and human

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(e.g. farm machinery) vectors (Bor, 1960; Ridley, 1930; Steel et al., 1983; Wilson, 1980). The retrorsely barbed setae of S. verticillata stick easily to animals and humans facilitating their dispersal (Bor, 1960).

The Setaria seed rain period in the north temperate regions of the world occur generally from July through December, depending on seasonal environmental conditions (notably the time of soil freezing and killing frost at the end of the season) and harvesting (Atchison, 2001; Haar, 1998; Peters et al., 1963; Stevens, 1960). The time of seed rain is continuous, with the seeds from 1° panicles occurring first, followed by 2° and subsequent tillers. On individual panicles, the seed rain progresses in approximately the order in which they flower (Dekker et al., 1996)

The numbers and yield of seed produced by a weedy Setaria plant is highly plastic, and strongly dependent on biomass accumulation, plant tillering and fascicle architecture (Haar, 1998; Kawano and Miyake, 1983). Setaria plant biomass is strongly dependent on available resources, competition from neighbors, and the time of seedling emergence. In general, plant size and seed number is greater for plants emerging earlier in the growing season than later (Schreiber, 1965b). Reports of seed productivity therefore vary from 1 to 12,000 seeds/plant (Peters et al., 1963; Rominger, 1962; Slife, 1954; Steel et al., 1983; Vanden Born, 1971). Seed number per panicle, panicle length and seed number per unit panicle length (seed density) were found to vary among Setaria species (S. faberii, S. viridis, S. glauca), panicle types (1°, 2°, 3°) and field locations (Haar,1998). For example, Haar (1998) found seed number per panicle varied by Setaria species, location and panicle type: S. faberii, 165 to 2127; S. viridis subsp. viridis, 144 to 725; and S. glauca, 54 to 213.

Because the weedy Setaria spp. seed rain is continuous over a weeks-to-months period, productivity can be underestimated by infrequent collection methods and inefficient capture techniques. Attempts to provide experimental seed productivity estimates (e.g. relationship between panicle length and seed number per unit length measurements) have produced inconclusive results (Barbour and Forcella, 1996; Defelice et al., 1989; Fausey et al., 1997; Haar, 1998).

CONCLUSIONS

The past history of the Setaria sp.-gp clearly indicates that invasion and local adaption is a continuous, ongoing process. Fifty-five years ago S. faberii was unknown in North American maize fields, now it's distribution is widespread. Setaria is highly adapted to exploit new opportunities provided by changes in management practices.

Selection, adaptation and the consequential evolution will continue to determine the future of the Setaria species-group. Weed management and the activities of humans are fundamental selection forces shaping and determining the conditions of existence of this group. The traits and adaptations that surviving weedy Setaria plants acquire in this struggle will continue to be the immediate problems managers confront. Therefore, weed and Setaria management is the management of weed selection pressures.

The past, present and future of the Setaria sp.-gp emphasizes the need for accurate predictions of future Setaria behavior. From a weed management and crop production perspective, the biggest needs for weedy Setaria spp. information is accurate predictions of seedling emergence, yield losses due to foxtail infestations, and seed return to the soil when they

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escape control. New information, integrated with that already existing, will guide management decisions based on economics, risk and sustainability

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