the role of trehalose 6-phosphate in crop yield and resilience · 3/28/2018 · 23. modification,...

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Short Title: Update on trehalose 6-phosphate signalling 1

Title: The role of trehalose 6-phosphate in crop yield and resilience 2

Matthew J. Paul*, Asier Gonzalez-Uriarte, Cara A. Griffiths, and Keywan Hassani-Pak 3

Plant Science, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, United Kingdom 4

ORCID IDs: 0000-0002-2001-961X (M.J.P.); 0000-0002-4159-6096 (A.G.); 0000-0001-5167-2606 5

(C.A.G.); 0000-0001-9625-0511 (K H-P). 6

*Address correspondence to [email protected] 7

Author Contributions: A. G. and K. H-P performed sequence and phylogenetic analysis; M.J.P. and 8 C.A.G wrote the paper, which all authors edited and approved 9

One sentence summary: T6P can be targeted through genetic and chemical methods for crop yield 10 improvements in different environments through the effect of T6P on carbon allocation and 11 biosynthetic pathways 12

Significant increases in global food security require improving crop yields in favourable and 13 poor conditions alike. However, it is challenging to increase both the crop yield potential and yield 14 resilience simultaneously, since the mechanisms that determine productivity and stress tolerance are 15 typically inversely related. Carbon allocation and use may be amenable to improving yields in a range 16 of conditions. The interaction between trehalose 6-phosphate (T6P) and SnRK1 (SNF1-related/AMPK 17 protein kinases) significantly affects the regulation of carbon allocation and utilisation in plants. 18 Targeting T6P appropriately to certain cell types, tissue types, and developmental stages results in an 19 increase in both yield potential and resilience. Increasing T6P levels promotes flux through 20 biosynthetic pathways associated with growth and yield, whereas decreasing T6P levels promotes 21 mobilisation of carbon reserves and movement of carbon associated with stress responses. Genetic 22 modification, gene discovery through QTL mapping, and chemical intervention approaches have been 23 used to modify the T6P pathway and improve crop performance under favourable conditions, drought, 24 and flooding in the three main food security crops: wheat (Triticum aestivum), maize (Zea mays), and 25 rice (Oryza sativa). Interestingly, both trehalose phosphate synthase (TPS) and trehalose phosphate 26 phosphatase (TPP) genes are associated with maize domestication. A phylogenetic comparison of 27 wheat TPS and TPP with eudicots and other cereals shows strong distinctions in wheat in both gene 28 families. This update highlights recent research examining the potential of the trehalose pathway in 29 crop improvement, and highlights an emerging strategy to increase cereal yields by targeting T6P in 30 reproductive tissue. 31

SUCROSE AND TREHALOSE: THE YIN AND YANG OF CROP IMPROVEMENT 32 Plants are the only organisms that synthesise both non-reducing disaccharides, trehalose and 33

sucrose. The ubiquity of both pathways in plants has been known for less than 20 years and was a 34 major revelation for those working on carbon metabolism, as well as plant scientists in general, given 35 the range of processes affected by the trehalose pathway. Plant metabolism is highly regulated. Part 36 of this regulation is through trehalose 6-phosphate (T6P) signalling that regulates metabolism in the 37 light of carbon availability and reprograms metabolism between anabolic or catabolic pathways 38 depending on the carbohydrate status of the plant. This discovery is also significant for understanding 39 the regulation of growth and development by carbon supply. Furthermore, the trehalose pathway may 40 widely impact crop improvement. Crops are not yet optimised to maximize their biosynthetic pathways 41 for yield in sinks and growth recovery that are promoted by high T6P, and for mobilisation of reserves 42 and sugar transport which can enable resilience that are promoted by low T6P. 43

Both the trehalose and sucrose biosynthesis pathways draw from a pool of core metabolites, 44 from which the carbon skeletons for all cellular components are also made (Paul et al. 2008). Flux 45

Plant Physiology Preview. Published on March 28, 2018, as DOI:10.1104/pp.17.01634

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through the trehalose pathway is more than a 1000-fold lower than the sucrose pathway. The low 46 abundance of both T6P and trehalose meant that T6P and trehalose did not show up in analytical 47 methods that were used to measure other sugars and sugar phosphates. It was not until more 48 sensitive methods were developed e.g. (Solanum tuberosum) (Roessner et al. 2000) that T6P and 49 trehalose could be more routinely detected. Subsequently, several laboratories have established 50 procedures to measure the abundance of T6P and trehalose (Lunn et al. 2006; Carillo et al. 2013; 51 Delatte et al. 2009; Delatte et al. 2011; Mata et al. 2016). The capacity to synthesise trehalose in 52 plants began to become apparent as the associated plant genes were identified (Blazquez et al. 1998; 53 Vogel et al. 1998). Subsequent publication of the Arabidopsis genome showed an abundance of both 54 trehalose phosphate synthase (TPS) and trehalose phosphate phosphatase (TPP) gene families with 55 11 and 10 members respectively (Leyman et al. 2001). 56 It is likely that T6P is a specific signal indicating sucrose abundance (Lunn et al. 2006; Nunes 57 et al. 2013a). T6P and sucrose levels are correlated in many tissues e.g. Arabidopsis and wheat 58 (Lunn et al. 2006; Martinez-Barajas et al. 2011) with the abundance of T6P being three orders of 59 magnitude lower than sucrose. Increases in sucrose from an endogenous or exogenous source leads 60 to a rapid induction of T6P in Arabidopsis (Lunn et al. 2006; Nunes et al. 2013). The mechanistic 61 details of this induction are not completely known but could involve sucrose regulation of TPS1 62 expression, which increases linearly in response to sucrose at low endogenous sucrose levels (Nunes 63 et al. 2013c). TPS5 is strongly induced by sucrose while other TPSs (TPS8-11) are strongly 64 repressed by sucrose, yet their roles in regulating T6P levels remain unknown. Heterologous 65 expression of AtTPS2 and AtTPS4 in the tps1 and tps2 yeast mutants, restore the yeasts’ ability to 66 synthesise T6P and trehalose (Delorge et al. 2015). However, these TPSs are not widespread in 67 species outside of the brassicaceae, so the broader significance of TPS2 and TPS4 in T6P synthesis 68 is unclear. The transcription factor bZIP11 induced by sucrose starvation induces the promoters of 69 TPP5 and TPP6 and of trehalase (TRE1) (Ma et al. 2011) which may be important in controlling T6P 70 levels under low carbon supply. All TPPs are likely catalytic (Vandesteene et al. 2012) whereas only 71 TPS1 and AtTPS2 and AtTPS4 out of 11 TPSs in Arabidopsis are catalytic. The functions of the other 72 TPSs have yet to be resolved. 73

Interestingly, prior to the discovery of T6P, research on glucose signalling through hexokinase 74 had already shown how a sugar signalling mechanism might operate. Hexokinase senses glucose 75 availability via a mechanism that is distinct from its catalytic function (Jang et al. 1997). Plants do not 76 synthesise glucose directly in photosynthesis; glucose is a product of the catabolism of sucrose, 77 starch, and cell wall carbohydrates, whereas sucrose is directly made through photosynthesis and, as 78 transportable carbon, is the starting point for provision of carbon for the synthesis of all plant 79 components. Hence glucose and sucrose signalling are likely to represent different avenues for crop 80 improvement. A mechanism that senses sucrose and regulates the use of sucrose can potentially 81 integrate photosynthesis with the use of sucrose to coordinate source and sink activities, a powerful 82 means of crop improvement already exemplified (Paul et al. 2017, see later). 83 84 CONSTITUTIVE EXPRESSION OF THE TREHALOSE PATHWAY IN TRANSGENIC PLANTS 85

Shortly before the discovery of active plant trehalose pathway enzymes (Blazquez et al. 1998; 86 Vogel et al. 1998) E. coli trehalose pathway genes had been transformed into plants to use plants as 87 a vehicle for trehalose production and improve drought tolerance through the accumulation of 88 trehalose (Goddijn et al. 1997). Trehalose was thought to be a key component that protects 89 resurrection plants, such as Selaginella species (Zentella et al. 1999; Iturriaga et al. 2000) and 90 Myrothamnus flabellifolius (Muller al. 1995) from desiccation as an osmolyte. As a non-reducing 91 disaccharide trehalose is stable and unreactive and accumulates to high levels in fungi, bacteria, 92 insects, and arthropods, where it doubles as a carbon store and protection compound in some cases 93 and was proposed as a target to improve drought tolerance in crops. The E. coli gene otsA encoding 94 TPS and otsB encoding TPP were heterologously expressed in the model plants Nicotiana tabacum 95 (Goddijn et al. 1997) and Arabidopsis thaliana (Schluepman et al. 2003). Very little trehalose 96 accumulated, but the transgenic plants displayed healthy and robust phenotypes (Schluepmann et al. 97



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2003; Pellny et al. 2004). This contrasted with the phenotypes of many other transgenic plants where 98 metabolism had been targeted, which either had impaired growth and development or had no effect 99 on phenotype compared with wild type plants (Paul et al. 2001). 100

101 102 To explain this, it was proposed that the trehalose pathway was engaging somehow with 103

endogenous regulatory or signalling mechanisms that linked carbon supply with the regulation of plant 104 growth and development. This also represented a strategy to modify carbon metabolism and resource 105 allocation to improve crop yield (Paul et al. 2001). 106

Constitutive heterologous expression of trehalose pathway genes in plants was a valuable 107 tool to establish the importance of the pathway, particularly of T6P, as a powerful regulator linking 108 metabolism with growth and development. For example, the earliest demonstration of the requirement 109 of T6P for carbohydrate utilisation in plants (Schluepmann et al. 2003), links to abscisic acid (ABA) 110 and auxin signalling (Avonce et al. 2004; Paul et al. 2010), as well as the activation of starch 111 synthesis (Kolbe et al. 2005) and breakdown (low T6P) (Martins et al. 2013). The wide-ranging impact 112 on metabolic pathways through inhibition of the protein kinase SnRK1 (SNF1-related/AMPK protein 113 kinases) (Zhang et al. 2009) was also shown which is discussed below. Experiments using an 114 ethanol-inducible promoter have also shown that organic and amino acid metabolism are regulated 115 through post-translational activation of nitrate reductase and phosphoenolpyruvate carboxylase in 116 Arabidopsis rosettes (Figueroa et al. 2016). There have also been several reports showing 117 improvements in stress tolerance in plants with constitutively expressed trehalose pathway genes, 118 with a notable example in rice (Garg et al. 2002), but this has not transferred to field cultivation. It has 119 not been possible to increase trehalose contents to provide significant osmoprotection, but trehalose 120 may promote the autophagy that is associated with drought tolerance (Williams et al. 2015). 121 Alternatively, changes in T6P levels may be responsible for improved stress tolerance, although 122 measurements of T6P rarely accompany studies, which limits understanding of the mechanistic basis 123 of enhanced drought tolerance obtained by modifying the pathway. Interestingly, a study of trehalose 124

contents in the drought-tolerant crops cassava (Manihot esculenta), Jatropha curcas, and castor bean 125

(Ricinus communis) showed far higher levels of trehalose, particularly in leaves, than has generally 126 been reported. This study reported up to 3 µmol of trehalose per gram fresh weight (Han et al. 2016) 127 compared to values that are usually more than 100-fold lower, in the tens of nmol per gram fresh 128 weight. Trehalose levels also appeared to be related to dehydration stress tolerance in detached 129 leaves and trehalose increased in response to osmotic stress. It is possible that a wider survey of 130 species with different environmental adaptions could show a stronger link between trehalose levels 131 and drought tolerance than has more generally been appreciated. Levels of trehalose itself could 132 reflect flux through the pathway rather than necessarily implicating a direct involvement of trehalose in 133 drought tolerance, which may be regulated by T6P. Interestingly, a comparison of two Selaginella 134 species that vary in drought tolerance showed that the drought-resistant species contained less 135 trehalose than the susceptible species (Pampurova et al. 2014), so the relationship between trehalose 136 accumulation and drought tolerance is not at all clear. In yeast, the TPS1 protein itself, and not 137 trehalose, is proposed to mediate stress tolerance (Petitjean et al. 2016). 138

For a major regulatory pathway, while constitutive expression of transgenes has given 139 valuable new insight, constitutive promoters are too much of a blunt instrument with which to 140 understand the subtleties of the cell, including the tissue- and developmental-specific nature of 141 regulation of metabolism by T6P. This is crucial not only for a mechanistic understanding, but also for 142 crop improvement. TPS and TPP gene expression is under strong cell-, tissue-, developmental-, and 143 environmental-specific regulation (Schluepmann and Paul 2009; Paul et al. 2008). Martinez et al. 144 (2011) showed strong tissue- and developmental-specific changes in T6P contents in wheat grain 145 during development. T6P is found in both maternal and paternal tissues at high levels up to 10 days 146 after anthesis, but is restricted to the endosperm beyond this period despite the sustained levels of 147 sucrose in maternal tissues. Hence, the role of T6P as a signal of sucrose availability (Lunn et al. 148 2006) has a strong developmental context. It is highly unlikely that superior crops with genetically 149



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modified trehalose pathway will emerge without appreciating and targeting T6P-dependent regulation 150 in a cell- and developmental-specific manner. 151

TARGETED EXPRESSION OF THE TREHALOSE PATHWAY IN TRANSGENIC MAIZE 152 Targeted expression (as opposed to constitutive expression discussed above) of a TPP gene 153

in maize is a striking example of how the pathway might be modified to improve crop performance. 154 Water availability is the primary factor affecting crop yields worldwide. For many crops, including 155 cereals, water deficit during the transition to reproductive development has the greatest impact on 156 yield by reducing grain set and hence final grain numbers. For example, maize kernel numbers can 157 be largely preserved during drought if they are supplied with sucrose (Zinselmeier et al. 1995; Boyer 158 and Westgate 2004). Combined with emerging knowledge about the function of T6P in regulating 159 carbohydrate use in plants (Schluepmann et al. 2003), and the known relationship between the 160 trehalose pathway and drought tolerance (Garg et al. 2002), Nuccio et al. (2015) put forward a 161 strategy to target the pathway in reproductive tissue during the flowering period. When using a 162 MADS6 promoter, which is active during flowering in reproductive tissue, to drive expression of a TPP 163 gene, substantial improvements in grain set and yields were achieved during droughts of different 164 severities during flowering (Nuccio et al. 2015). Furthermore, yield was increased even without 165 drought. It is likely that grain abortion is a survival strategy to ensure that at least some kernels 166 survive when resources are limiting. The plant has no way of knowing how severe the drought will be 167 and, in many cases, more grains are aborted than is necessary. Increasing the sucrose contents of 168 developing kernels with this genetic modification (GM) approach represents a strategy to achieve 169 higher yields under drought and is one of few examples where GM has improved drought tolerance 170 that has been thoroughly tested in field conditions with no yield penalty under optimal hydration. 171 Interestingly, drought tolerance in this example is improved by targeting carbon allocation rather than 172 directly targeting water use efficiency. This work to target T6P in maize reproductive tissue began 173 before more recent insights on the mechanistic mode of action of T6P through SnRK1 signalling were 174 available (Zhang et al. 2009). 175

176 MECHANISTIC BASIS OF CROP YIELD IMPROVEMENT FROM TARGETING T6P 177

Much of the fundamental work on T6P signalling has been conducted in Arabidopsis. This has 178 provided a good framework for understanding the function of the pathway and will continue to be an 179 invaluable tool. In fact, an ideal discovery/ crop improvement programme would include Arabidopsis 180 alongside crops given the Arabidopsis genetic resources and ease of cultivation and experimentation 181 in this species. Many of the discoveries regarding the function of T6P in Arabidopsis will also hold true 182 in crops because of the central and conserved function of the pathway. However, a major limitation of 183 Arabidopsis is that it does not have any large sinks. Sink tissues of tubers, fruit, seeds, and grain form 184 the majority of harvested crop produce. Furthermore, because of the absence of large sinks in 185 Arabidopsis, source-sink relations may be less sophisticated in Arabidopsis than in crops where a 186 large proportion of carbon is partitioned to harvested sinks. Hence, this process needs to be studied 187 in crops for crop improvement and to appreciate the full role of T6P in plant processes. For example, 188 whilst some of the general principles behind targeting T6P to improve drought tolerance in maize 189 (Nuccio et al. 2015) came from understanding that T6P regulates carbon utilisation in Arabidopsis 190 (Schluepmann et al. 2003), this had to accompany knowledge of the development of reproductive 191 sinks in maize. 192

One notable difference between Arabidopsis and cereals is the level of T6P. In Arabidopsis, 193 T6P levels can reach 10 nmol g

-1 fresh weight (FW) T6P in seedlings (Nunes et al. 2013a) although 194

typically levels are tenfold lower, and another order of magnitude lower in rosettes (Lunn et al. 2006). 195 Additionally, 119 nmol T6P g

-1 FW has been reported in the wheat grain endosperm (Martinez et al. 196

2011). Maize kernels contain up to 50 nmol T6P g-1

FW (Nuccio et al. 2015; Bledsoe et al. 2017). 197 There are currently no T6P measurements in rice grain, although the concentration of T6P is 198 expected to be as high as in other cereals. A T6P:sucrose nexus has been proposed, which may 199 differ across tissues and species (Yadav et al. 2014). The basis of this nexus is that sucrose induces 200 T6P biosynthesis which then drives down sucrose levels by promoting sucrose consumption through 201



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metabolism, storage, growth, and development. In crops, domestication may indeed have changed 202 this nexus. Interestingly, whilst T6P appears to consistently correlate with sucrose in Arabidopsis it 203 does not always do so in wheat when T6P levels are resolved in specific tissue levels during various 204 developmental stages. In wheat grain T6P is found at high levels in paternal and maternal tissues 205 during early development up to 10 days after anthesis. After this stage, T6P becomes confined to the 206 endosperm, even though sucrose levels are still high pericarp tissues showing that development and 207 tissue type can override direct effects of sucrose on T6P levels (Martinez et al. 2011). In maize, after 208 returning culture kernels from starvation to sucrose-rich conditions, direct correlations between 209 sucrose and T6P levels become much weaker, suggesting complex regulation of T6P levels beyond 210 the effects of sucrose that are not yet fully understood (Bledsoe et al. 2017). It is possible that there is 211 some deregulation of the T6P:sucrose nexus in crops that have been selected for in breeding, which 212 may be necessary for high yields. In wheat and maize, the T6P:sucrose ratio is lower than in 213 Arabidopsis. It is possible that the catalytic machinery for the synthesis and breakdown of T6P, 214 sensing T6P, or the downstream interaction with SnRK1, gives rise to a lower T6P:sucrose nexus. 215

Inhibition of SnRK1 by T6P provides a framework for understanding the mode of action of 216 T6P and for many of the wide-ranging effects of modifying T6P in plants (Zhang et al. 2009) including 217 providing a basis for the T6P:sucrose nexus. SnRK1 is a member of the conserved AMPK, SNF1-218 related protein kinases that regulates energy- and carbon availability-related processes in all 219 eukaryotic organisms. SnRK1 regulates enzyme activities directly by changing their phosphorylation 220 states (Halford et al. 2003) and regulates gene expression (Baena-Gonzalez et al. 2007). The bZIP11 221 transcription factor may be particularly important in this regard (Ma et al. 2011; Delatte et al. 2011). 222 T6P inhibits the catalytic activity of SnRK1 to relieve the inhibition of growth and development by 223 SnRK1, thus enabling growth to proceed in the presence of adequate carbon. Biosynthetic pathway 224 and growth genes that are repressed by SnRK1 are derepressed by T6P, whereas stress and 225 catabolic pathway genes that are induced by SnRK1 are repressed by T6P. In this way, T6P provides 226 the “licensing factor”, as it has been described, for sucrose utilisation in plants (Smeekens et al. 227 2015). Inhibition of SnRK1 by T6P has been shown in Arabidopsis in vitro protein kinase assays that 228 measure SnRK1 catalytic activity with and without T6P (Zhang et al. 2009) and can be inferred in 229 SnRK1 overexpression lines, which rescue plant growth on high trehalose and hence which overcome 230 T6P inhibition of SnRK1 in these conditions (Delatte et al. 2011). Catalytic assays also show SnRK1 231 inhibition by T6P in crops (Wu and Birch, 2010, sugar cane; Debast et al. 2011, potato; Martinez-232 Barajas et al. 2011, wheat; Nuccio et al. 2015, maize; Zhang et al. 2015, cucumber). SnRK1 marker 233 genes were identified in the pioneering work of Baena-Gonzalez et al. (2007) and these were shown 234 to change in a manner consistent with T6P-mediated changes in SnRK1 activity in vivo in transgenic 235 Arabidopsis with altered T6P content (Zhang et al. 2009). A similar pattern emerged when 236 Arabidopsis seedlings were exposed to different environmental treatments that affected T6P levels 237 (Nunes et al. 2013). Relationships between SnRK1 marker genes and T6P have also been shown in 238 wheat (Martinez-Barajas et al. 2011) and maize (Henry et al. 2015; Bledsoe et al. 2017). T6P inhibits 239 SnRK1 in all actively growing tissues, while in mature leaves SnRK1 is largely insensitive to inhibition 240 by T6P (Zhang et al. 2009). This fits a paradigm where T6P and SnRK1 coordinate sucrose usage 241 with anabolic growth and development. In Arabidopsis seedlings, the inhibition constant (Ki) of T6P 242 for SnRK1 is around 5 µM (Nunes et al. 2013b), whereas in wheat and maize grain it is about 50 µM 243 (Martinez et al. 2011; Nuccio et al. 2015). For non-competitive inhibitors, such as T6P, Ki is the 244 concentration of inhibitor required for 50% inhibition. The different SnRK1 Kis in crops compared to 245 Arabidopsis could be due to crop domestication. 246

Recently, important insight was obtained on how changes in T6P levels in transgenic maize 247 (Nuccio et al. 2015) results in a larger grain set and higher yields (Oszvald et al. 2018). Dissection of 248 female reproductive tissues expressing the MADS6-TPP construct showed that changes in T6P 249 produces outcomes that are highly tissue specific. Two- to three-fold decreases in T6P produced by 250 this construct resulted in similar changes in gene expression for metabolic pathways in component 251 tissues of developing maize cobs, downregulating primary metabolic pathways (sucrose, starch, 252 amino acids), but upregulating secondary metabolic pathways (lipids and endogenous trehalose). 253



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However, this produced different effects on metabolite distribution in florets compared to the pith 254 tissue that supplies the florets. Florets accumulated sucrose and amino acids at the expense of the 255 pith. This was related to the upregulation of several SWEET genes in the pith and florets, and to the 256 maintenance of higher rates of photosynthesis for longer in leaves. This could form the basis for a 257 molecular mechanism of source-sink relations. The transgene was found to localize to the phloem 258 vasculature and companion cells. Altering T6P in the phloem could mediate changes in sucrose 259 transport via T6P/ SnRK1-regulated SWEET proteins. This also stimulated photosynthesis in leaves 260 (Oszvald et al. 2018). This provides an exciting model for source-sink relations that can be tested and 261 developed in crop improvement (Fig. 1). In support of this, TPS1 and bZIP11 expression are 262 associated with phloem vasculature (Genevestigator, https://genevestigator.com/gv/; Lastdrager et al. 263 2014). Oszvald et al. (2018) also showed changes in SnRK1 activity, SnRK1 subunit composition, 264 and expression of SnRK1 marker genes, together with striking changes in endogenous trehalose 265 pathway genes, which suggest mutual T6P/SnRK1 regulation as part of a feedback loop. 266

267 NATURAL VARIATION IN TPP GENES UNDERLYING IMPORTANT CROP TRAITS 268

Ramosa 3 (RA3) was one of the earliest examples of a trehalose pathway gene affecting a 269 crop trait (Satoh-Nagasawa et al. 2006). Maize has both male and female reproductive structures with 270 different architectures that were selected during maize domestication to enhance its utility as an 271 agricultural crop. The male inflorescence, or tassel, has long branches at its base and a central spike 272 that bears shorter branches containing spikelet pairs. The female inflorescences are positioned 273 laterally and contain only short branches, a trait that is thought to aid in the efficient packing and 274 harvesting of seeds. RA3 is required for this specialized architecture, because ra3 mutant tassels 275 have additional long branches and ra3 mutant ears have abnormally long branches at their bases. 276 RA3 encodes a TPP which regulates inflorescence branching and is expressed in discrete domains 277 subtending axillary inflorescence meristems. RA3 may regulate inflorescence branching by 278 modification of T6P or a target of T6P that moves into axillary meristems. However, alteration of T6P 279 concentrations by RA3 has not been shown because of the difficulties in measuring T6P in very small 280 discrete tissue samples. Alternatively, RA3 itself may have a transcriptional regulatory function. 281 A TPP represents a quantitative trait locus in rice for germination under anaerobic conditions 282 (Kretzschmar et al. 2015). The primary way of cultivating rice is in flooded paddy fields and the ability 283 to germinate well in such conditions has been a sought-after trait. Directly seeding rice into flooded 284 fields would remove the necessity for labour intensive transplantation of rice plants. Efficient use of 285 starch reserves is crucial in coping with energy starvation and maintaining growth under anaerobic 286 germination. Kretzschmar et al. (2015) identified a functional TPP7 gene in a genomic region, qAG-9-287 2, that associated with tolerance of anaerobis during germination. TPP7 likely contributes to 288 anaerobic germination tolerance by modulating and decreasing local T6P levels, which leads to 289 enhanced starch mobilization through amylase activation. The flux of sugars toward the sink is 290 promoted, providing the energy and carbon necessary for coleoptile growth under anaerobic 291 conditions. 292

A wheat TPP has recently been found to be associated with grain weight in bread wheat 293 (Zhang et al. 2017). Using recombinant inbred lines derived from parents with high and low thousand 294 grain weight (TGW), a SNP in a promoter region of a TPP gene (TaTPP-6AL1) was identified that is 295 significantly associated with TGW. Differential expression and alteration of T6P levels, likely in the 296 reproductive tissues, may confer TGW variation in wheat. This gene could be used as a selection 297 marker to increase wheat yield potential. 298

So far, TPP genes are the only trehalose pathway genes that are known to affect crop 299 improvement. No TPS genes have been associated with crop traits. Interestingly, based on the 300 genome-wide resequencing of 75 wild landrace and improved maize lines, both TPS and TPP genes 301 are listed as genes associated with domestication improvement (Hufford et al. 2012). It is of great 302 interest to determine whether closely associated genes are present in other important crops such as 303 wheat, how domestication has affected these, and what further selection may be possible. This 304


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suggests that both TPSs and TPPs could be targeted in crop improvement programmes including 305 wheat. 306

307 PHYLOGENETIC ANALYSIS OF WHEAT TPS AND TPP GENES 308

We conducted phylogenetic comparison of the TPS and TPP gene families using the genome 309 sequences available in Ensembl Plants release 38 (http://plants.ensembl.org/index.html) for 310 Arabidopsis, Oryza sativa (Japonica rice), Brachypodium distachyon, Zea mays (maize), Glycine max 311 (soybean), and Triticum aestivum (bread wheat) (Fig. 2, 3). Arabidopsis TPS and TPP genes 312 (Leyman et al. 2001) were used as a query to identify orthologues in these species using the Ensembl 313 Plants BioMart portal (http://plants.ensembl.org/biomart/martview; Smedley et al. 2015). Additionally, 314 Ensembl Plants release 38 was searched for genes annotated with the TPP (IPR003337) constituent 315 domain to avoid missing more divergent genes. Genes were classified as TPSs if they contained a 316 glycosyl transferase family 20 (IPR001830) domain and as TPPs if they only had the phosphatase 317 domain as described in Leyman et al. (2001) and Lunn (2007) (Supplementary Figures 1, 2 and 318 Supplementary Tables 1, 2). Using this approach, we identified 99 plant TPS genes and 100 TPPs 319 but manual investigation of gene length, structure and domain composition suggested that several 320 plant trehalose pathway genes were not complete or were incorrectly annotated in their respective 321 genome versions (Supplementary Tables 3, 4). Therefore, genes that were more divergent than the 322 E. coli otsA and otsB genes that were used as outgroups (data not shown) were not included in the 323 final analysis. Similarly, the E. coli genes were removed from the final tree to improve legibility. In 324 addition, the wheat protein sequences belonging to the TGACv1 wheat reference (Clavijo et al. 2017) 325 were improved (Supplementary Tables 5, 6) performing BLAST searches in an in-house TimeLogic® 326 DeCypher® server (tera-blastp, max_scores = 10, evalue ≤ 1-5) against the high-confidence IWGSC 327 RefSeq v1.0 proteins (available under Toronto agreement). Using this methodology, we have 328 identified 25 wheat TPS proteins (Supplementary Tables 7, 9) and 33 TPPs (Supplementary Tables 8, 329 10). 330

The reconstructed evolutionary story is markedly different for TPS and TPP genes but there 331 are some common features. With a few exceptions, genes of the two eudicot species (Arabidopsis 332 and soybean) clustered together more closely than the genes of the four monocot species, supporting 333 the ancestral origin of the genes as divergent evolution after the monocot-eudicot separation. Within 334 the monocots, the clusters tended to have one B. distachyon gene very closely related to three wheat 335 homeologues, as expected because the former is considered the closest fully sequenced wild relative 336 of wheat. In addition, one rice gene and two maize genes (old tetraploid) usually clustered with them. 337 This pattern is quite consistent within the TPS phylogenetics tree (Fig. 2) but is more variable among 338 the TPPs (Fig. 3). The TPS tree is divided into two main clades as noted by several authors (Lunn 339 2007; Henry et al. 2014; Xie et al 2015; Han et al. 2016). Class I includes TPSs with a high number of 340 exons (minimum of 9 but usually more than 15, Supplementary Table 4a). In contrast to previous 341 studies, we found that the Arabidopsis class I TPS genes did not separate into two subgroups 342 (AtTPS1 and AtTPS2-AtTPS4) but rather clustered together with five soybean genes, suggesting that 343 expansion of the class I genes may be a feature of the eudicots as it also happens in cassava (Han et 344 al. 2016). Interestingly, wheat had two class I gene sets totalling seven genes that were all on 345 chromosome 1. It seems that the most divergent set of genes had four homeologues instead of three 346 due to a potential tandem duplication in chromosome 1D (Supplementary Table 9). The class II TPSs 347 can be further divided into four clades with distinct monocot-eudicot features. AtTPS11 had a single 348 orthologue in wheat, which is surprising given that B. distachyon had two genes in the same clade 349 and rice and maize have even more. AtTPS5 and AtTPS6 formed a common clade with two wheat, 350 two B. distachyon, and two maize genes. The TPS7 gene was extended as a family in monocots, with 351 three wheat, B. distachyon, and rice genes. The two maize genes (Zm00001d043468 and 352 Zm00001d043469) closest to AtTPS7 are genes associated with domestication improvement (Table 353 1, Fig. 2, Hufford et al. 2012). The TPS8-10 clade appears to have had a varied fate in the different 354 monocots, with no wheat genes, a single B. distachyon gene, and multiple rice and maize genes. 355 Zm00001d032311 is another maize gene associated with domestication improvement (Hufford et al. 356


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2012). TPP genes have diversified even more, with most clades being characteristic to either 357 monocots or eudicots (Fig. 3). Some authors (Henry et al. 2014; Xie et al 2015; Han et al. 2016) 358 divide TPPs into two clades (A and B), mainly based on the Arabidopsis TPPs clustering into two 359 groups but only clade A, which includes AtTPPA, F, and G seems to be conserved in all species. 360 Clade B (AtTPPB, C, D, E, H, I, and J) was more diverse and was divided into an exclusively eudicot 361 clade and three monocot-exclusive clades. Interestingly, one of the monocot-only clades had three 362 wheat genes with three homeologues each, all of them on chromosome 2. Zm00001d032298 is 363 another gene associated with maize domestication improvement (Hufford et al. 2012). There was also 364 an isolated clade that contained four wheat and three soybean proteins that were more related to the 365 ancestral bacterial otsB protein (not shown in tree). However, caution is required when interpreting 366 this clade since three of the four wheat genes were longer than average and also encoded a Gnk2-367 homologue fungal resistance domain (Supplementary Tables 8, 10). The differing gene numbers 368 across the species could be an evolutionary sign of the flexibility of trehalose biosynthesis genes, with 369 each of them having specialised roles in different species although artefacts due to problems with 370 genome assemblies and annotations cannot still be ruled out due to the nascent nature of sequence 371 information for wheat. A more detailed expression analysis is needed to confirm the inferred functions 372 of these wheat genes. 373 374 CHEMICAL INTERVENTION OF T6P 375

Genetic methods using natural variation or genetic modification of the trehalose pathway 376 show great promise for crop improvement. A recent complementary development is chemical 377 intervention with T6P, which can serve as an additional tool for perturbing T6P levels, identifying new 378 genes, and probing for further detail of the mechanistic basis of T6P signalling (Griffiths et al. 2016). 379 T6P in its native form does not cross membranes. Griffiths et al. (2016) showed that applying T6P 380 precursors synthesised using phosphorus chemistries to attach light-labile chemical groups that 381 enable uptake of T6P, but which are then cleaved away in sunlight or ultra-violet light to release T6P 382 and increase endogenous T6P levels more than 100-fold. One 1 mM spray which delivered a pulse of 383 T6P 10 days after anthesis had the effect of increasing grain size and yield at harvest a month later. 384 Much can be gained by increasing T6P well above normal physiological limits. The role of T6P in 385 starch synthesis and biosynthetic pathways had already been shown (Kolbe et al. 2005; Zhang et al. 386 2009) and the stimulation of starch synthesis by T6P suggests that the capacity for starch synthesis in 387 grain currently imposes a limitation on wheat yields. T6P primes gene expression for starch 388 biosynthesis and stimulating sink capacity in such a way is a promising route to yield improvement. 389

T6P also stimulates biosynthesis in other ways. Transfer of plants from cold to warm results in 390 a growth spurt following the transfer. It was shown that T6P primes gene expression for this growth 391 stimulation (Nunes et al. 2013a). Following this precedent, the T6P precursors were also used to see 392 if recovery from drought could be enhanced. In this instance, new growth and resurrection of existing 393 growth was stimulated by T6P precursors when applied 1 day before re-watering after a 9-day 394 drought period (Griffiths et al. 2016). This suggests that T6P is a general stimulator of biosynthetic 395 pathways that are attenuated in a tissue-dependent manne including starch synthesis in the wheat 396 endosperm and other biosynthetic pathways including cell walls in vegetative tissue that are required 397 for regrowth. This can be explained through the wide-ranging repressive effects of SnRK1 on 398 biosynthetic pathways (Baena-Gonzalez et al. 2007) that are derepressed by T6P (Zhang et al. 2009). 399 In addition to pushing physiological boundaries for yield and recovery from drought, chemical 400 intervention provides other advantages. Whereas promoter gene constructs are fixed, chemical 401 applications are flexible. A T6P spray can be applied at particular developmental stages and 402 environmental conditions. This chemical spray could potentially be used for a range of crops. It would 403 need to be tested to ensure that there are no adverse effects, for example, on the susceptibility to 404 pathogens, since sugar signalling is known to play an important role in plant–pathogen interactions 405 (Morkunas and Ratajczak 2014). However, increasing T6P and trehalose contents may actually be 406 beneficial in this regard (Tayeh et al. 2014). There are other chemicals that can be used in the 407 chemical intervention of plant growth, particularly plant hormones such as auxin, gibberellin, ethylene, 408



9

and compounds that can oppose the effects of the hormones (Santner et al. 2009). However, T6P is 409 the only growth regulator known that directly targets sugar signalling, sucrose use, and sucrose 410 allocation. 411 412 OVERALL EMERGINGING MODEL FOR MODIFYING T6P FOR CROP IMPROVEMENT 413 Drawing on the significant yield improvements achieved in maize carrying MADS6-TPP 414 (Nuccio et al. 2015; Oszvald et al. 2018) and chemical intervention in wheat (Griffiths et al. 2016), a 415 strategy can be proposed for targeting T6P to reproductive tissue to improve yield. Decreasing T6P in 416 the phloem vasculature that supplies the developing grain with sucrose would increase sucrose 417 import into the grain by upregulating SWEET gene expression. Increasing T6P in the grain 418 endosperm itself would promote starch biosynthesis within the grain, according to the example with 419 T6P precursors in wheat (Griffiths et al. 2016; Fig. 4). Additionally, selection of TPS and TPP genes 420 has occurred during maize domestication (Hufford et al. 2012; Table 1). Investigating the roles of 421 these genes in other cereals may be particularly promising moving forward. Manipulating genes such 422 as rice TPP7 may confer better performance in different environments such as flooded rice fields 423 (Kretzschmar et al. 2015). Orphan crops may be particularly amenable to improvement of the 424 trehalose pathway given the domestication improvements seen in maize. Genetic and chemical 425 intervention can be used as complementary methods to target T6P. As a central regulator of source 426 sink whose optimisation and synchrony is essential for efficiency of carbon generation and utilisation 427 for crop yields, T6P is likely to feature strongly in future crop yield and resilience improvement 428 programmes. 429 430 ACKNOWLEDGEMENTS 431

Rothamsted Research receives strategic funding from the Biotechnological and Biological 432 Sciences Research Council of the United Kingdom. We acknowledge BBSRC grants BB/C51257X/1, 433 BB/D006112/1 (SCIBS) and BB/N004205/1 (SARIC) and support through the 20:20 wheat and 434 designing future wheat (DFW) strategic programmes (BB/P016855/1). 435

436



10

437

Cereal gene Closest Arabidopsis gene

Putative physiological role

Close gene in wheat

Close gene in rice

Close gene in maize

Zm00001d043468 TPS7

Improvement candidates in maize (Hufford et al. 2012). No known function

√ √

Zm00001d043469

Zm00001d032311 TPS8-10 Improvement candidate in maize (Hufford et al. 2012). No known function

no √

TraesCS6A01G248400 TPPA, F, G

Likely catalytic function, associated with grain weight (Zhang et al. 2017)

√ √

TraesCS6B01G276300

TraesCS6D01G230500

Os09T0369400 TPP7 Distinct cereal TPP clade

Likely catalytic function, enables germination under anoxia through starch mobilisation (Kretzschmar et al. 2015)

√ √

Zm00001d022193 Distinct cereal TPP clade

Ramosa3, role in inflorescence architecture (Satoh-Nagasawa et al. 2006)

√ √

Zm00001d032298 Distinct cereal TPP clade

Improvement candidate in maize (Hufford et al. 2012); likely catalytic function

√ √

Table 1. TPS and TPP genes associated with domestication improvements in maize (from Hufford et 438 al. 2012) and with improvements in specific crop traits in wheat, rice, and maize. 439

440



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FIGURE LEGENDS 441

Figure 1. Mechanistic framework for regulation of source-sink relations mediated by T6P/ SnRK1. 442 T6P tracks sucrose levels. T6P inhibits SnRK1 which regulates key genes for involved in allocation 443 (SWEETs) and use (starch biosynthesis) of sucrose. Enhanced use of sucrose stimulates carbon 444 fixed in photosynthesis. A feedback loop likely operates where SnRK1 phosphorylates bZIP11 which 445 regulates expression of TPPs; other TPSs are regulated by SnRK1 as established SnRK1 marker 446 genes. Proteins in orange boxes, carbohydrates in yellow boxes. 447 Figure 2. Phylogenetic tree of TPS proteins. Arabidopsis thaliana (AT, dark green), Glycine max 448 (soybean, GLYMA, purple), Brachypodium distachyon (BRADI, brown), Oryza sativa Japonica (rice, 449 OS, light blue), Zea mays (maize, Zm, light green) and Triticum aestivum (bread wheat, TraesCS, 450 orange). Full length TPS protein sequences were aligned using MUSCLE v3.8.425 (Edgar 2004) with 451 default parameters as part of the Geneious tool suite (version 10.0.9, https://www.geneious.com, 452 Kearse et al. 2012) and gaps were manually removed. Maximum likelihood trees were constructed 453 using PHYML (Guidon et al. 2010) with 1000 bootstraps and implementing the default LG amino acid 454 substitution model (Le and Gascuel 2008). The scale bar represents 0.4 amino acid substitutions per 455 site. Trees have been depicted using the tree viewer in Geneious and edited using Inkscape. 456 Figure 3. Phylogenetic tree of TPP proteins. Arabidopsis thaliana (AT, dark green), Glycine max 457 (soybean, GLYMA, purple), Brachypodium distachyon (BRADI, brown), Oryza sativa Japonica (rice, 458 OS, light blue), Zea mays (maize, Zm, light green) and Triticum aestivum (bread wheat, TraesCS, 459 orange). Full length TPP protein sequences were aligned using MUSCLE v3.8.425 (Edgar 2004) with 460 default parameters as part of the Geneious tool suite (version 10.0.9, https://www.geneious.com, 461 Kearse et al. 2012) and gaps were manually removed. Maximum likelihood trees were constructed 462 using PHYML (Guidon et al. 2010) with 1000 bootstraps and implementing the default LG amino acid 463 substitution model (Le and Gascuel 2008). The scale bar represents 0.4 amino acid substitutions per 464 site. Trees have been depicted using the tree viewer in Geneious and edited using Inkscape. 465 Figure 4. Model for modification of T6P levels to increase yield in cereal reproductive tissue. 466 Elevation of T6P levels in cereal grain increases starch biosynthesis and grain size. A decrease in 467 T6P in phloem companion cells increases SWEET gene expression and sucrose efflux into the grain. 468 469 SUPPLEMENTARY DATA 470 Supplementary Figure 1: Domain structure of a complete plant TPS protein (using AtTPS1 as a 471 model). 472 Supplementary Figure 2: Domain structure of a complete plant TPP protein (using AtTPPA as a 473 model). 474 Supplementary Table 1: Constitutive domains of TPS proteins. 475 Supplementary Table 2: Constitutive domains of TPP proteins. 476 Supplementary Table 3: Summary of the structural information of the TPS genes and proteins. 477 Available for E. coli, A. thaliana, soybean, B. distachyon, rice, maize and wheat. 478 Supplementary Table 4: Summary of the structural information of the TPP genes and proteins. 479 Available for E. coli, A. thaliana, soybean, B. distachyon, rice, maize and wheat. 480 Supplementary Table 5: Transformation of the wheat TGACv1 TPS transcript ids into IWGSC 481 RefSeq v1.0 ids using tera-blastp. 482 Supplementary Table 6: Transformation of the wheat TGACv1 TPP transcript ids into IWGSC 483 RefSeq v1.0 ids using tera-blastp. 484 Supplementary Table 7: Functional annotation of the identified wheat TPS proteins according to the 485 IWGSC RefSeq 1.0 reference. 486 Supplementary Table 8: Functional annotation of the identified wheat TPP proteins according to the 487 IWGSC RefSeq 1.0 reference. 488 Supplementary Table 9: Chromosomal coordinates of the wheat TPS genes (in gff3 format) plus 489 structural information. 490

Supplementary Table 10: Chromosomal coordinates of the wheat TPP genes (in gff3 format) plus 491 structural information. 492


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Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul MJ (2003) Trehalose 6-phosphate is 646 indispensable for carbohydrate utilisation and growth in Arabidopsis thaliana. Proceedings of National 647 Academy of Sciences 100, 6849-6854 648 Smedley D, Haider S, Durinck S, Pandini L, Provero P, Allen J et al. (2015) The Biomart 649 community portal: an innovative alternative to large centralised data repositories. Nucleic Acids 650 Research 43,589-598 651 Smeekens S (2015) From Leaf to Kernel: Trehalose-6-Phosphate Signaling Moves Carbon in the 652 Field. Plant Physiology DOI: https://doi.org/10.1104/pp.15.01177 653 Tayeh C, Randoux B, Vincent D, Bourdon N, Reignault P (2014) Exogenous trehalose induces 654 defenses in wheat before and during a biotic stress caused by powdery mildew. Phytopathology 655 104:293-305. doi: 10.1094/PHYTO-07-13-0191-R 656 Vandesteene L, Lopez-Galvis L, Vanneste K, Feil R, Maere S, Lammens W, Rolland F, Lunn JE, 657 Avonce N, Beeckman T, Van Dijck P (2012) Expansive evolution of the trehalose -6-phosphate 658 phosphatase gene family in arabidopsis. Plant Physiol 160, 884-896 659 Vogel G, Aeschbacher RA, Muller J, Boller T, Wiemken A (1998) Trehalose 6-phosphate 660 phosphatases from Arabidospis thaliana: identification by functional complementation of yeast tps2 661 mutant. Plant J 13, 673-683 662 Williams B, Njaci I, Moghaddam L, Long H, Dickman MB, Zhang X, Mundree S (2015) Trehalose 663 accumulation triggers autophagy during plant desiccation. PLOS Genetics doi: 664 10.1371/journal.pgen.1005705 665 Wu L and Birch RG (2010) Physiological basis for enhanced sucrose accumulation in an engineered 666 sugarcane cell line. Funct Plant Biol 37, 1161-1174 667 Xie DW, Wang XN, Fu LS, Sun J, Zheng W, Li ZF (2015) Identification of the trehalose-6-phosphate 668 synthase gene family in winter wheat and expression analysis under conditions of freezing stress. 669 Journal of Genetics, 94(1), 55–65. https://doi.org/10.1007/s12041-015-0495-z 670 Yadav UP, Ivakov A, Feil R, Duan G-Y, Walther D, Giavalisco P, Piques M, Carillo P, 671 Hubberten H-M, Stitt M, Lunn JE (2014) The sucrose trehalose-6-phosphate (T6P) nexus: specificity 672 and mechanisms of sucrose signalling by T6P. Journal Experimental Botany 65, 1051-1068 673 Zentella R, Mascorro-Gallardo JO, Van Dijck P, Folch-Mallol J, Bonini B, Van Vaeck C, Gaxiola 674 R, Covarrubias AA, Nieto-Sotelo J, Thevelien JM, Iturriaga G (1999) A Selaginella lepidophylla 675 trehalose 6-phosphatase synthase complements growth and stress-tolerance defects in a yeast tps1 676 mutant. Plant Physiology 119, 1473-1482 677 Zhang Z, Deng Y, Song X, Miao M (2015) Trehalose 6-phosphate and SNF1-related protein kinase1 678 are involved in the first fruit inhibition of cucumber. J Plant Phys 177, 110-120 679 Zhang Y, Primavesi LF, Jhurreea D, Mitchell R, Powers S, Schluepmann H, Delatte T, Wingler 680 A, Paul MJ (2009) Inhibition of Snf1-related protein kinase (SnRK1) activity and regulation of 681 metabolic pathways by trehalose 6-phosphate. Plant Physiology 149, 1860-1871 682 Zhang P, He Z, Tian X, Gao F, Xu D, Liu J, Wen W, Fu L, Li G, Sui X, Xia X, Wang C, Cao S 683 (2017) 684 Cloning of TaTPP-6AL1 associated with grain weight in bread wheat and development of functional 685 marker. Mol Breeding doi 10.1007/s11032-017-0676-y 686 Zinselmeier C, Lauer MJ, Boyer JS (1995) Reversing drought-induced losses in grain yield: sucrose 687 maintains embryo growth in maize. Crop Science 35, 1390-1400 688


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https://www.ncbi.nlm.nih.gov/pubmed/?term=Randoux%20B%5BAuthor%5D&cauthor=true&cauthor_uid=24073639

https://www.ncbi.nlm.nih.gov/pubmed/?term=Vincent%20D%5BAuthor%5D&cauthor=true&cauthor_uid=24073639

https://www.ncbi.nlm.nih.gov/pubmed/?term=Bourdon%20N%5BAuthor%5D&cauthor=true&cauthor_uid=24073639

https://www.ncbi.nlm.nih.gov/pubmed/?term=Reignault%20P%5BAuthor%5D&cauthor=true&cauthor_uid=24073639

http://jxb.oxfordjournals.org/search?author1=Alexander+Ivakov&sortspec=date&submit=Submit

http://jxb.oxfordjournals.org/search?author1=Regina+Feil&sortspec=date&submit=Submit

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http://jxb.oxfordjournals.org/search?author1=Dirk+Walther&sortspec=date&submit=Submit

http://jxb.oxfordjournals.org/search?author1=Patrick+Giavalisco&sortspec=date&submit=Submit

http://jxb.oxfordjournals.org/search?author1=Maria+Piques&sortspec=date&submit=Submit

http://jxb.oxfordjournals.org/search?author1=Petronia+Carillo&sortspec=date&submit=Submit

http://jxb.oxfordjournals.org/search?author1=Petronia+Carillo&sortspec=date&submit=Submit

http://jxb.oxfordjournals.org/search?author1=Hans-Michael+Hubberten&sortspec=date&submit=Submit

http://jxb.oxfordjournals.org/search?author1=Hans-Michael+Hubberten&sortspec=date&submit=Submit


T6P

bZIP11

SWEETs

Sucrose

TPS TPP

Sucrose

Starch Trehalose

Photosynthesis

Enhanced demand for sucrose

Enhanced demand for sucrose

SnRK1

Figure 1. Mechanistic framework for regulation of source-sink relations mediated by T6P/ SnRK1. T6P tracks sucrose levels. T6P inhibits SnRK1 which regulates key genes for involved in allocation (SWEETs) and use (starch biosynthesis) of sucrose. Enhanced use of sucrose stimulates carbon fixed in photosynthesis. A feedback loop likely operates where SnRK1 phosphorylates bZIP11 which regulates expression of TPPs; other TPSs are regulated by SnRK1 as established SnRK1 marker genes. Proteins in orange boxes, carbohydrates in yellow boxes



Figure 2. Phylogenetic tree of TPS proteins. Arabidopsis thaliana (AT, dark green), Glycine max (soybean, GLYMA, purple), Brachypodium

distachyon (BRADI, brown), Oryza sativa Japonica (rice, OS, light blue), Zea mays (maize, Zm, light green) and Triticum aestivum (bread wheat,

TraesCS, orange). Full length TPS protein sequences were aligned using MUSCLE v3.8.425 (Edgar 2004) with default parameters as part of the

Geneious tool suite (version 10.0.9, https://www.geneious.com, Kearse et al. 2012) and gaps were manually removed. Maximum likelihood trees

were constructed using PHYML (Guidon et al. 2010) with 1000 bootstraps and implementing the default LG amino acid substitution model (Le and

Gascuel 2008). The scale bar represents 0.4 amino acid substitutions per site. Trees have been depicted using the tree viewer in Geneious and

edited using Inkscape.




Figure 3. Phylogenetic tree of TPP proteins. Arabidopsis thaliana (AT, dark green), Glycine max

(soybean, GLYMA, purple), Brachypodium distachyon (BRADI, brown), Oryza sativa Japonica (rice, OS, light

blue), Zea mays (maize, Zm, light green) and Triticum aestivum (bread wheat, TraesCS, orange). Full length TPP

protein sequences were aligned using MUSCLE v3.8.425 (Edgar 2004) with default parameters as part of the

Geneious tool suite (version 10.0.9, https://www.geneious.com, Kearse et al. 2012) and gaps were manually

removed. Maximum likelihood trees were constructed using PHYML (Guidon et al. 2010) with 1000 bootstraps

and implementing the default LG amino acid substitution model (Le and Gascuel 2008). The scale bar

represents 0.4 amino acid substitutions per site. Trees have been depicted using the tree viewer in Geneious

and edited using Inkscape. www.plantphysiol.orgon October 22, 2020 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.



Targeting of T6P in cereal reproductive tissue for yield improvement

Elevate T6P in kernels

Inhibited SnRK1 Feast response

Promotion of starch biosynthetic capacity

Promotion of sucrose movement to kernels

SWEETS

Active SnRK1 Famine response

Yield 20% in wheat (Griffiths et al. 2016) Yield 9-123% in maize

(Nuccio et al. 2015; Oszvald et al. 2018)

Increased allocation and conversion

of sucrose to starch in grain

Decrease T6P in phloem

companion cells

Sink-led photosynthetic carbon gain

pith

Figure 4. Model for modification of T6P levels for higher yield in cereal reproductive tissue. Elevation of T6P levels in cereal grain increases starch biosynthesis and grain size. Decrease in T6P in phloem companion cell increases SWEET gene expression and sucrose efflux into grain.



ADVANCES

• T6P can be targeted to improve yield potential and resilience to diverse stresses by regulating whole-plant carbohydrate allocation and utilization.

• Promoting carbohydrate allocation and utilization in sinks by optimizing T6P increases photosynthesis.

• Increasing T6P promotes biosynthetic pathways associated with grain yield, such as starch synthesis, while decreasing T6P promotes resource mobilization and changes in sucrose allocation, enabling better performance under abiotic stress.

• Expressing a TPP gene with a MAD6S promoter in maize shows how drought tolerance can be improved in the field without imposing a yield penalty under well-watered conditions.

• Genetic variation in TPP genes is associated with traits including grain weight and germination under anaerobic conditions.

• Chemical intervention of T6P increases grain size when applied to grain and promotes recovery of vegetative tissue after drought, most likely through gene priming for these traits.



OUTSTANDING QUESTIONS

• How has domestication already changed the trehalose and SnRK1 pathways and what additional changes to T6P/ SnRK1 signaling can be made to further improve crop traits?

• What are the functions of the many TPS and TPP genes in wheat and other crops?

• What are the SnRK1, TPS, and TPP signaling complexes composed of?

• What are the T6P targets beyond SnRK1? • What is the function of trehalose?



Parsed CitationsAvonce N, Leyman B, Mascorro-Gallardo JO, van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose 6-phosphatesynthase AtTPS1 gene is a regulator of glucose, abscisic acid and stress signalling. Plant Physiol 136, 3649-3659

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energysignalling. Nature 448, 938-942


Blazquez MA, Santos E, Flores C-L, Martinez-Zapater JM, Salinas J, Gancedo C (1998) Isolation and molecular characterisation of theArabidopsis TPS1 gene, encoding a trehalose phosphate synthase. Plant J 13, 685-689


Bledsoe SW, Henry C, Griffiths CA, Paul MJ, Feil R, Lunn JE, Stitt M, Lagrimini LM (2017) The role of Tre6P and SnRK1 in maize earlykernel development and events leading to stress-induced kernel abortion. BMC Plant Biology doi 10.1186/s12870-017-1018-2


Boyer JS, Westgate ME (2004) Grain yields with limited water. Journal of Experimental Botany 55, 2385-2394Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Carillo P, Feil R, Gibon Y, Satoh-Nagasawa N, Jackson D, Bläsing OE, Stitt M, Lunn JE (2013) A fluorometric assay for trehalose in thepicomole range. Plant Methods DOI: 10.1186/1746-4811-9-21


Clavijo BJ, Venturini L, Schudoma C, Accinelli GG, Kaithakottil G, Wright J et al. (2017). An improved assembly and annotation of theallohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomaltranslocations. Genome Research, 27, 885–896.


Debast S, Nunes-Nesi A, Hajirezaei MR, Hofmann J, Sonnewald U, Fernie AR, Börnke F (2011) Altering trehalose-6-phosphate contentin transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiol. 156, 1754-1771


Delorge I, Figueroa CM, Feil R, Lunn JE, Van Dijck P (2015) Trehalose 6-phosphate synthase 1 is not the only active TPS in Arabidopsisthaliana. Biochem J 466 283-290


Delatte TL, Sedijani P, Kondou Y, Matsui M, de Jong GJ, Somsen GW, Wiese-Klinkenberg A, Primavesi LF, Paul MJ, Schluepmann H(2011) Growth arrest by trehalose-6-phosphate: an astonishing case of primary metabolite control over growth by way of the SnRK1signaling pathway. Plant Physiology 157, 160-174


Delatte TL, Selman MHJ, Schluepmann H, Somsen GW, Smeekens SCM, de Jong GJ (2009) Determination of trehalose 6-phosphate inArabidopsis seedlings by successive extraction by anion exchange chromatography mass spectrometry. Analytical Biochemistry 389,12-17


Edgar RC (2004) MUSCLE: multiple sequences alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792-1797

Pubmed: Author and Title www.plantphysiol.orgon October 22, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

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Nuccio ML Wu J, Mowers R, Zhou H, Meghji M, Primavesi LF, Paul MJ, Chen X, Gao Y, Haque E, Basu S, Lagrimini LM (2015)Expression of trehalose 6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. NatureBiotechnology 33, 862-869


Nunes C, O’Hara L, Primavesi LF, Delatte TL, Schluepmann H, Somsen GW, Silva AB, Fevereiro PS, Wingler A, Paul MJ (2013a) TheT6P/ SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiology 162, 1720-1732


Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ, Sagar R, Fevereiro PS, Davis BG, Paul MJ (2013b) Inhibition ofSnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiology and Biochemistry 63, 89-98


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Oszvald M, Primavesi LF, Griffiths CA, Cohn J, Basu SS, Nucio ML, Paul MJ (2018) Trehalose 6-phosphate in maize reproductivetissue regulates assimilate partitioning and photosynthesis. Plant Physiology, doi.org/10.1104/pp.17.01673


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Paul MJ, Oszvald M, Jesus C, Rajulu C, Griffiths CA (2017) Increasing crop yield and resilience with trehalose 6-phosphate: targeting afeast-famine mechanism in cereals for better source-sink optimisation. J Ex Bot doi:10.1093/jxb/erx083


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http://www.ncbi.nlm.nih.gov/pubmed?term=Morkunas I%2C Ratajczak L %282014%29 The role of sugar signaling in plant defense responses against fungal pathogens%2E Acta Physiol Plant %282014%29 36%3A1607�??1619 DOI 10%2E1007%2Fs11738%2D014%2D1559%2Dz&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Nunes C%2C O�??Hara L%2C Primavesi LF%2C Delatte TL%2C Schluepmann H%2C Somsen GW%2C Silva AB%2C Fevereiro PS%2C Wingler A%2C Paul MJ %282013a%29 The T6P%2F SnRK1 signaling pathway primes growth recovery following relief of sink limitation%2E Plant Physiology 162%2C 1720%2D1732&dopt=abstract

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Biol 37, 1161-1174Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Xie DW, Wang XN, Fu LS, Sun J, Zheng W, Li ZF (2015) Identification of the trehalose-6-phosphate synthase gene family in winter wheatand expression analysis under conditions of freezing stress. Journal of Genetics, 94(1), 55–65. https://doi.org/10.1007/s12041-015-0495-z


Yadav UP, Ivakov A, Feil R, Duan G-Y, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten H-M, Stitt M, Lunn JE (2014) Thesucrose trehalose-6-phosphate (T6P) nexus: specificity and mechanisms of sucrose signalling by T6P. Journal Experimental Botany 65,1051-1068


Zentella R, Mascorro-Gallardo JO, Van Dijck P, Folch-Mallol J, Bonini B, Van Vaeck C, Gaxiola R, Covarrubias AA, Nieto-Sotelo J,Thevelien JM, Iturriaga G (1999) A Selaginella lepidophylla trehalose 6-phosphatase synthase complements growth and stress-tolerance defects in a yeast tps1 mutant. Plant Physiology 119, 1473-1482


Zhang Z, Deng Y, Song X, Miao M (2015) Trehalose 6-phosphate and SNF1-related protein kinase1 are involved in the first fruitinhibition of cucumber. J Plant Phys 177, 110-120


Zhang Y, Primavesi LF, Jhurreea D, Mitchell R, Powers S, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of Snf1-related protein kinase (SnRK1) activity and regulation of metabolic pathways by trehalose 6-phosphate. Plant Physiology 149, 1860-1871


Zhang P, He Z, Tian X, Gao F, Xu D, Liu J, Wen W, Fu L, Li G, Sui X, Xia X, Wang C, Cao S (2017)

Cloning of TaTPP-6AL1 associated with grain weight in bread wheat and development of functional marker. Mol Breeding doi10.1007/s11032-017-0676-y

Zinselmeier C, Lauer MJ, Boyer JS (1995) Reversing drought-induced losses in grain yield: sucrose maintains embryo growth in maize.Crop Science 35, 1390-1400



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http://www.ncbi.nlm.nih.gov/pubmed?term=Xie DW%2C Wang XN%2C Fu LS%2C Sun J%2C Zheng W%2C Li ZF %282015%29 Identification of the trehalose%2D6%2Dphosphate synthase gene family in winter wheat and expression analysis under conditions of freezing stress%2E Journal of Genetics%2C 94%281%29%2C 55�??65%2E https%3A%2F%2Fdoi%2Eorg%2F10%2E1007%2Fs12041%2D015%2D0495%2Dz&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Xie&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Identification of the trehalose-6-phosphate synthase gene family in winter wheat and expression analysis under conditions of freezing stress&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Identification of the trehalose-6-phosphate synthase gene family in winter wheat and expression analysis under conditions of freezing stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xie&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yadav UP%2C Ivakov A%2C Feil R%2C Duan G%2DY%2C Walther D%2C Giavalisco P%2C Piques M%2C Carillo P%2C Hubberten H%2DM%2C Stitt M%2C Lunn JE %282014%29 The sucrose trehalose%2D6%2Dphosphate %28T6P%29 nexus%3A specificity and mechanisms of sucrose signalling by T6P%2E Journal Experimental Botany 65%2C 1051%2D1068&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yadav UP, Ivakov A, Feil R, Duan G-Y, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten H-M, Stitt M, Lunn JE (2014) The sucrose trehalose-6-phosphate (T6P) nexus: specificity and mechanisms of sucrose signalling by T6P. Journal Experimental Botany 65, 1051-1068

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Yadav&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The sucrose trehalose-6-phosphate (T6P) nexus: specificity and mechanisms of sucrose signalling by T6P&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The sucrose trehalose-6-phosphate (T6P) nexus: specificity and mechanisms of sucrose signalling by T6P&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yadav&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zentella R%2C Mascorro%2DGallardo JO%2C Van Dijck P%2C Folch%2DMallol J%2C Bonini B%2C Van Vaeck C%2C Gaxiola R%2C Covarrubias AA%2C Nieto%2DSotelo J%2C Thevelien JM%2C Iturriaga G %281999%29 A Selaginella lepidophylla trehalose 6%2Dphosphatase synthase complements growth and stress%2Dtolerance defects in a yeast tps1 mutant%2E Plant Physiology 119%2C 1473%2D1482&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zentella R, Mascorro-Gallardo JO, Van Dijck P, Folch-Mallol J, Bonini B, Van Vaeck C, Gaxiola R, Covarrubias AA, Nieto-Sotelo J, Thevelien JM, Iturriaga G (1999) A Selaginella lepidophylla trehalose 6-phosphatase synthase complements growth and stress-tolerance defects in a yeast tps1 mutant. Plant Physiology 119, 1473-1482

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zentella&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A Selaginella lepidophylla trehalose 6-phosphatase synthase complements growth and stress-tolerance defects in a yeast tps1 mutant&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A Selaginella lepidophylla trehalose 6-phosphatase synthase complements growth and stress-tolerance defects in a yeast tps1 mutant&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zentella&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Z%2C Deng Y%2C Song X%2C Miao M %282015%29 Trehalose 6%2Dphosphate and SNF1%2Drelated protein kinase1 are involved in the first fruit inhibition of cucumber%2E J Plant Phys 177%2C 110%2D120&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Z, Deng Y, Song X, Miao M (2015) Trehalose 6-phosphate and SNF1-related protein kinase1 are involved in the first fruit inhibition of cucumber. J Plant Phys 177, 110-120

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Trehalose 6-phosphate and SNF1-related protein kinase1 are involved in the first fruit inhibition of cucumber&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Trehalose 6-phosphate and SNF1-related protein kinase1 are involved in the first fruit inhibition of cucumber&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang Y%2C Primavesi LF%2C Jhurreea D%2C Mitchell R%2C Powers S%2C Schluepmann H%2C Delatte T%2C Wingler A%2C Paul MJ %282009%29 Inhibition of Snf1%2Drelated protein kinase %28SnRK1%29 activity and regulation of metabolic pathways by trehalose 6%2Dphosphate%2E Plant Physiology 149%2C 1860%2D1871&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang Y, Primavesi LF, Jhurreea D, Mitchell R, Powers S, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of Snf1-related protein kinase (SnRK1) activity and regulation of metabolic pathways by trehalose 6-phosphate. Plant Physiology 149, 1860-1871

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhang&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Inhibition of Snf1-related protein kinase (SnRK1) activity and regulation of metabolic pathways by trehalose 6-phosphate&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zinselmeier C%2C Lauer MJ%2C Boyer JS %281995%29 Reversing drought%2Dinduced losses in grain yield%3A sucrose maintains embryo growth in maize%2E Crop Science 35%2C 1390%2D1400&dopt=abstract

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http://scholar.google.com/scholar?as_q=Reversing drought-induced losses in grain yield: sucrose maintains embryo growth in maize&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zinselmeier&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1


the role of trehalose 6-phosphate in crop yield and resilience · 3/28/2018 · 23. modification,...

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