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Agricultural and Forest Meteorology 232 (2017) 433–442

Contents lists available at ScienceDirect

Agricultural and Forest Meteorology

journa l homepage: www.e lsev ier .com/ locate /agr formet

esearch Paper

ow variable are non-linear developmental responses to temperaturen two perennial forage species?

erge Zaka, Lina Qadir Ahmed, Abraham J. Escobar-Gutiérrez, Franc ois Gastal,ernadette Julier, Gaëtan Louarn ∗

NRA UR4 URP3F, CS80006, F86600 Lusignan, France

r t i c l e i n f o

rticle history:eceived 8 April 2016eceived in revised form8 September 2016ccepted 2 October 2016

eywords:evelopmentrowthenetic variabilityemperaturelfalfa (Medicago sativa L.)all fescue (Festuca arundinacea schreb.)henotyping

a b s t r a c t

Developmental responses to temperature are critical to yield formation in crops and perennial grasslandspecies. However, their characterisation over a broad range of temperatures relevant to climate changestudies has been limited in these species. The present study sought to determine the non-linear devel-opmental responses to temperature of two major grassland species, tall fescue (Festuca arundinacea) andalfalfa (Medicago sativa), and to assess i) whether a coordinated response occurred between differentdevelopmental processes, ii) if genotypes from contrasting origins differed in their responses, and iii) toquantify how a lack of coordination and genetic variability might affect estimates of thermal time pro-gression under present and future climate scenarios. Two series of experiments were carried out undercontrolled conditions with eight constant temperatures ranging from 5 ◦C to 40 ◦C applied to seedlings andmature plants. Different growth and developmental processes were characterized, including shoot devel-opment and radicle, leaf and stem growth. Once normalized to a temperature of 20 ◦C, the temperatureresponses of the different processes displayed no significant variability between temperate and Mediter-ranean genotypes. On the other hand, not all developmental processes within a genotype displayed acoordinated response to temperature. Significant departures from the response of shoot development inmature plants were observed regarding several processes, particularly at low and supra-optimal temper-atures (up to ±5 ◦C and ±2 ◦C for minimal and maximal temperature estimates, respectively). Differences

were particularly marked relative to node and stem elongation responses. Overall, when using the tem-perature dependencies of different processes to estimate cumulative thermal time, significant bias wasobserved in alfalfa when considering stem elongation by comparison with other processes. The conse-quences for improvements to forage crop models, and for the meta-analyses often used to calibrate them,are discussed.

© 2016 Elsevier B.V. All rights reserved.

. Introduction

Temperature is one of the most important environmental factorsnvolved in the control of plant growth and development (Ritchiend Nesmith, 1991). It plays a major role in dynamic crop mod-ls, acting both as a variable that drives phenological developmentnd as an abiotic stress impeding specific physiological functionseyond determined thresholds (Brisson et al., 1998; Parent andardieu, 2014). Because of climate change, the average global tem-

erature is expected to rise by between 1.5 ◦C and 4.5 ◦C duringhe next century (IPCC, 2013), with marked impacts worldwide onhe yields of annual crops (Tubiello et al., 2007; Challinor et al.,

∗ Corresponding author.E-mail address: gaetan.louarn@inra.fr (G. Louarn).

ttp://dx.doi.org/10.1016/j.agrformet.2016.10.004168-1923/© 2016 Elsevier B.V. All rights reserved.

2009; Schlenker and Roberts, 2009) and grasslands (Soussana andLüscher, 2007; Brisson and Levrault, 2010; Ruget et al., 2013). How-ever, considerable uncertainties remain concerning these projectedimpacts, in part due to how the temperature sensitivity of cropspecies and genotypes is represented and parameterized in cur-rent models (Zhang et al., 2008; Lobell and Burke, 2008; Parent andTardieu, 2014).

Developmental responses to temperature (i.e. those whichdefine the rate at which the plant cycle progresses and plant tis-sues expand) are critical to yield formation because they affect theduration of the crop cycle, the expansion of leaf area and roots, andthe overall fit between crop development and resource availability.

All crop and grassland models consider temperature-compensatedtime (i.e. thermal time or normalized days; Bonhomme, 2000;Parent et al., 2010) as driving progression of the plant cycle andcontrolling organ expansion directly, or indirectly through pho-

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34 S. Zaka et al. / Agricultural and Fo

osynthesis and carbon allocation (Parent and Tardieu, 2014).owever, these models differ in the degree of simplification used toccount for temperature dependency (ranging from linear to multi-inear or curvilinear relationships), and in the distinction madeetween processes regarding a coordinated response to temper-ture. Curvilinear models show the best fit to actual physiologicalates over a broad range of temperatures (Yin et al., 1995; Yan andunt, 1999). However, in the past, most models were implementedsing simpler linear functions (Jamieson et al., 1998; Brisson et al.,998) and parametrized over a narrow range of temperaturesypical of present-day temperate areas. Parameters determiningon-linear transitions, such as optimum and maximum develop-ental rates, have been shown to exert a strong influence under

uture climate projections (Challinor et al., 2005; Zhang et al.,008; Ceglar et al., 2011). A series of studies sought to determinehe relevant parameters required to calibrate improved non-linearesponses in several annual crops (Porter and Gawith, 1999; Parentt al., 2010; Parent and Tardieu, 2012). But despite their agronomicnd environmental importance, the responses of perennial grass-and species have received much less attention to date (Brown et al.,005).

Determining temperature dependency over the whole temper-ture range experienced by a species is detailed and costly work.or this reason, many characterizations have focused on eitherimited temperature ranges (Garcia-Huidobro et al., 1982; Covellt al., 1986; Ellis et al., 1986; Gastal et al., 1992), short-term growthesponses (seedling growth, Masiunas and Carpenter, 1984; leaflongation, Sadok et al., 2007) or short duration phases (e.g. ger-ination; Sakanoue, 2010; Dürr et al., 2015). Specific response

urves have often been derived using a meta-analysis to gatherormalized data from different experiments and genotypes (Dellt al., 2011; Parent and Tardieu., 2012). In particular, it has beenrgued that different genotypes within a species generally have aommon temperature dependency, and that several physiologicalrocesses present similar, seemingly coordinated, responses (Yannd Hunt, 1999 in maize; Parent and Tardieu, 2012 in 17 annualrop species). These propositions differ strikingly from the com-on assumptions made in perennial grassland species to explain

arietal differences in the seasonality of production (Cooper, 1964;obson and Jewis, 1968; Nelson et al., 1978) or in the germinationate of natural populations (Ahmed, 2015). In particular, intra-pecies differences in temperature response were hypothesizedy Cooper (1964) to explain the genotype by season interactionsually observed between growth rates when comparing temper-te and Mediterranean cultivars (i.e. Mediterranean cultivars growore rapidly during spring and autumn but more slowly during

ummer; Cooper, 1964; Robson and Jewiss, 1968; McLaughlin andhristie, 1980; Lelièvre and Volaire, 1993; Volaire and Lelièvre,001; Volaire et al., 2009; Annicchiarico et al., 2013). However,etailed developmental responses have never been compared inuch plant materials. Furthermore, it is still unclear which develop-ental processes actually share a common temperature response,

nd if so which biological mechanisms might be involved. Contra-ictory results have been reported in the literature, indicating theossibility of significant differences in the cardinal temperaturesi.e. minimum, maximum and optimum temperatures at which

process occurs) of different developmental processes (Craufurdt al., 1998; Porter and Gawith, 1999). For instance, germinationnd early seedling growth rates were shown to display very dif-erent temperature responses in several perennial species (Ahmed,015).

In the present study, our overall objective was to characterise

he non-linear developmental responses of two major perennialorage species with a broad geographic distribution, namely tallescue and alfalfa. These two temperate grassland species present aroad phenotypic diversity and can cope with both cold winters and

eteorology 232 (2017) 433–442

hot dry summers (Buckner et al., 1979; Michaud et al., 1988). Theiruse is likely to increase in a context of climate change (Helgadóttiret al., 2016). Our aim was therefore to determine: i) if developmen-tal processes in seedlings and mature perennial plants present acoordinated temperature response, ii) if temperate and Mediter-ranean populations actually differ in terms of their responses totemperature, and iii) the quantified effects of these two sourcesof variations (process selection and genotype) on predictions ofthermal time progression under contrasting climate scenarios.

2. Materials and methods

2.1. Plant material

Two series of experiments were carried out using tall fescue(Festuca arundinacea Schreb.) and alfalfa (Medicago sativa L.). Oneseries was conducted on seedlings and the other on mature plants.In both cases, two cultivars (i.e. synthetic varieties containingsignificant genetic diversity, Julier et al., 2000) from contrastingthermal origins were studied in each species (Table 1). In order toovercome the genetic variability of cultivars and to perfectly repli-cate identical genotypes at different temperatures, four additionalclones selected along a north-south gradient of origin were charac-terized during the mature plant experiments. For alfalfa, the cloneswere propagated from stem cuttings and grown in a greenhouse forabout three months before the experiment. For tall fescue, cloneswere produced from individual tillers selected from a mother plantat the start of the experiment. Tall fescue mother plants were grownin a greenhouse with a 16 h photoperiod in order to ensure thatfloral induction did not occur and that selected tillers were at thevegetative stage during the experiments. For the sake of simplic-ity, cultivars and clones will be designated as genotypes in theremainder of this manuscript.

2.2. Seedling growth experiments

A series of eight independent experiments, one for each tem-perature treatment, was carried out sequentially under controlledgrowing conditions in two growth cabinets at INRA Lusignan,France. Seedling preparation was identical for all temperaturetreatments and included a wet-stratification (7 days at 5 ◦C for tallfescue) and seed scarification (alfalfa). A germination period wasassured for 48 h at 25 ◦C in the dark. When the radicle or coleop-tile/hypocotyl length was >2 mm, the seeds were considered tohave germinated and the seedlings were placed in germinationboxes over sheets of blue blotting-paper (Anchor Paper, St Paul,Minnesota). For each cultivar, three boxes containing ten seedlingswere then grown in the dark at temperatures ranging from 5 ◦C to40 ◦C. The temperature in the growth chamber was maintained at aconstant level (5 ◦C, 10 ◦C, 15 ◦C, 20 ◦C, 25 ◦C, 30 ◦C, 35 ◦C and 40 ◦Ctemperature treatments) with a high humidity (VPD < 1.5 kPa). Thegermination boxes were arranged according to a completely ran-domized design and placed at a 60◦ angle from horizontal. Theseedlings were irrigated regularly with sterile deionized water.Heterotrophic growth of the radicle was characterized for each cul-tivar at each temperature using image analysis. A Nikon D70 digitalcamera (60 mm lens, aperture f/2.8, Nikon, Tokyo, Japan) was usedto collect images at a resolution of 3008 × 2000 pixels (200 ISO).About 15 images of each box were taken at intervals adapted tothe growth temperature. The images were analysed using ImageJ

software (version 1.47, NIH, Bethesda, MD, http://imagej.nih.gov/ij/). Radicle lengths were determined using a combination of auto-mated and manual methods, with an internal standard to convertpixels into mm.

S. Zaka et al. / Agricultural and Forest Meteorology 232 (2017) 433–442 435

Table 1Origins and characteristics of the alfalfa and tall fescue cultivars and clones used.

Species Cultivar/clone Breeder Origins Beginning of vegetative growthb

Alfalfa Harpe cv. Verneuil Holding et Semunion(1996)

Temperate –

Alfalfa Barmed cv. Barenbrug Holland B.V. (2002) Mediterranean (North Africa) –Alfalfa Clone G3 from Orca cv.a Carneau Frères (1966) Temperate –Alfalfa Clone 7 7 from

Demnate landraceaMoroccan landrace Mediterranean (31◦43′N

7◦02′W)–

Alfalfa Clone 6 10 from Lodicv.a

Istituto Sperimentale ColtureForaggere, Lody, Italy

Mediterranean –

Alfalfa Clone 8 2 fromKrasnokutskayapopulationa

Wild population from Russia Continental (49◦15′N 41◦94′E) –

Tall fescue Soni cv. Jouffray-Drillaud SemencesINRA, France (2000)

Temperate 23/03

Tall fescue Centurion cv. Verneuil Holding et Semunion(1997)

Mediterranean (Morocco) 01/03

Tall fescue Clone 31 10 from Sonicv.

Jouffray-Drillaud SemencesINRA, France (2000)

Temperate 23/03

Tall fescue Clone 26 10 fromDauphine cv.

Semences de France, France(2005)

Temperate 22/03

Tall fescue Clone 25 10 fromCenturion cv.

Verneuil Holding et Semunion(1997)

Mediterranean (Morocco) 01/03

Tall fescue Clone 24 10 from Flexy RAGT (2002) Temperate 22/03

2

uacaivqedOdtavddAftt(p3tisTeadr

itswt

cv.

a selected from a collection of clones described in Maamouri et al. (2015).b http://www.herbe-book.org, consulted on 23th November 2015.

.3. Mature plant experiments

A second series of independent experiments was performednder a controlled environment using mature autotrophic plantst the vegetative stage. The plants were grown in an 8.1 m2 growthhamber (model 97132/7NU, Froids et Mesures, Beaucouzé, France)t eight air temperatures ranging from 5 ◦C to 40 ◦C with 5 ◦Cncrements. Seedlings and clone cuttings were transplanted indi-idually into 1.5L pots (10 × 30 cm cylindrical pots) filled with fineuartz (0.8–1.4 mm mesh). After transplantation, the pots (16 forach cultivar and four for each clone) were arranged in a ran-omized block design. Lights (POWERSTAR, HQI-BT 400WD lamps,SRAM, Munich, Germany) supplied a photosynthetic photon fluxensity (PPFD) of 400 to 450 �mol photon m−2 s−1 at pot levelhroughout a 14 h photoperiod. The pots were ferti-irrigated with

complete nutrient solution (Gastal and Saugier, 1989) at inter-als ranging from three times (5 ◦C) to eight times (35–40 ◦C) aay. Two growth phases were distinguished. First, a 3-week con-itioning period at 25 ◦C and 70% relative humidity was applied.t the five-leaf stage for alfalfa, and the three-leaf stage for tall

escue, plants were transferred to the studied growth tempera-ure for a period corresponding to five phyllochrones for alfalfa andhree phyllochrones for tall fescue. Daily average air temperaturesTgrowth) were adjusted so that the average daily meristem tem-eratures (Tapex) were equal to 5 ◦C, 10 ◦C, 15 ◦C, 20 ◦C, 25 ◦C, 30 ◦C,5 ◦C or 40 ◦C in alfalfa (Sup Tab A). Soil and meristem tempera-ures were recorded every minute with thermocouples and storedn a data-logger. The meristem temperature in tall fescue was mea-ured with a thermocouple fixed in the last sheath of the main tiller.his temperature was 2.5 ◦C higher than that of alfalfa meristems,xcept for the 5 ◦C treatment when the pots were covered withluminium foil to lower the soil temperature. The vapour pressureeficit (VPD) was kept below 1.5 kPa at all Tgrowth by adjusting theelative humidity.

At each temperature, measurements were performed at regularntervals with a ruler (every 24 to 72 h depending on the growth

emperature) in order to determine leaf, node and stem lengths on aample of shoots/tillers (Sup Table B). For alfalfa, the primary shootsere monitored. The leaves of phytomers ranked eight to ten, and

he internodes of phytomers ranked five to six, were measured. For

tall fescue, measurements were performed on leaves of the maintiller on ranks four to six. In addition, the number of visible leaveswas counted on each of the monitored shoots/tillers. A total of 16(internode elongation) to 32 (leaf elongation, shoot elongation andleaf appearance rates) shoot/tillers was measured for each cultivar,and a total of four shoot/tillers was monitored for each clone (SupTable B).

2.4. Determination of growth and leaf appearance rates

Leaf appearance rates (LER) and stem elongation rates (SER)were calculated for each shoot by fitting a linear model to the timeseries measurements of primary leaf number counts and primarystem lengths. The slope of the relationship over the whole periodat Tgrowth determined the rate. For leaf (LER), internode (IER) andradicle (RER) expansion rates, maximum rates were determined byfitting a logistic function to the time series measurements of eachorgan:

L = Lmax

1 + e�.(�−t)(1)

where L represents the organ length at time t, Lmax the final organlength, and � and � are two parameters accounting for maximumrates and delayed growth, respectively. The maximum growth ratewas determined as the first derivative at the 50% growth inflex-ion point. All fits were performed using the non-linear regressionfunction nls of R language (R development Core Team, 2005).

2.5. Determination of temperature dependencies

The three-parameter beta function described by Graux (2011)was used to fit the non-linear relationship between growth rates(f) and temperature (T) for the different processes and genotypesstudied:

if Tmin < T < Tmax : f (T) = RTref .

(T − TminTref − Tmin

)q

.

(Tmax − T

Tmax − Tref

)

if T ≤ TminorT ≥ Tmax : f (T) = 0 (2)

4 rest Meteorology 232 (2017) 433–442

Tipp((

T

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2

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2

battaidfwtb((

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Fig. 1. Examples of time dynamics of leaf appearance on the main stem (a) and leaflength (b) under the different temperature treatments studied. Data are for alfalfacv. Harpe. Measurements of leaf length concerned leaves on the phytomer #9. Linescorrespond to the model fits used to derive the maximum leaf appearance rate (LAR)and maximuml leaf elongation rate (LER).

36 S. Zaka et al. / Agricultural and Fo

his equation has three parameters: the minimum (Tmin) and max-mum (Tmax) temperatures at which a process occurs and q, a shapearameter. In the equation, Tref accounts for a fixed reference tem-erature (20 ◦C) andRTref , the rate at the reference temperatureequal to 1 for normalized responses). The optimum temperatureTopt) and the maximum rate (Rmax) were calculated as follows:

opt= 11 + q

(Tmin+q∗Tmax) (3)

max= f (Topt) (4)

This model was chosen following a preliminary model selectiontudy during which 23 temperature response models were com-ared regarding the most contrasted dependencies observed in ourataset (Sup Table C and D). Low Bayesian Information Criterionalues indicated the satisfactory ability of this model to define arade-off between the number of parameters used and the qualityf the fits (Schwarz, 1978).

.6. Model fitting

Model fits were performed using R software (https://www.r-roject.org/). The nls procedure was used to determine parame-ers from Eq. (1) and (2). Regarding temperature responses (Eq.2)), no constraints were imposed on the range of parameter val-es to ensure fitting convergence. To enable the combined analysisf different processes regardless of dimensions, units or absoluteate values, each process rate was normalized by the value of thebsolute rate at a reference temperature of 20 ◦C. The rate of allormalized curves was thus 1 at 20 ◦C (RTref set to 1).

.7. Comparison of temperature dependencies

Sequential pair-wise model comparisons were performedetween the fits of absolute (comparison of different genotypes for

given process) or normalized (comparison of different processes)emperature responses. For each couple of models compared, awo-sided Kolmogorov-Smirnov test (ks.test procedure) was firstpplied to test for the normal distribution of residuals when switch-ng datasets. A Student test (t.test procedure) was then applied toetermine any bias of the mean between the two models (mean dif-

erence assumed to be equal to 0). Finally, when the two first testsere successful, a lack-of-fit test (pf procedure) was performed to

est for significant differences between the model fits. The proba-ility of a calculated F-value being greater than that of a tabular FPr > F) was calculated and comparative matrices were constructedP < 0.01).

.8. Impact of model selection on the calculation ofemperature-compensated time

For each temperature dependency, temperature-compensatedimes were computed annually as the sum of equivalent days at0 ◦C (D20).

20 =365∑i=1

f (T)i (5)

here f (T)iwas the normalized growth rate for day i given by Eq.2) and T the arithmetic mean between the daily minimum and

aximum temperatures. Series of daily weather data from twoontrasting temperate (Lusignan, 46.43◦N, 0.12◦W) and Mediter-

anean (Avignon, 49.91◦N, 4.90◦W) locations were used for twoeriods (current 1980–2010 and future 2070–2100). The genera-ion of the daily meteorological data series was described by Brissonnd Levrault (2010), based on the IPCC A1B scenario.

3. Results

3.1. Effect of meristem temperature on the kinetics of shootdevelopment and organ growth

Fig. 1 presents examples of the time series measurements usedto determine shoot development and organ growth rates under thedifferent temperature treatments. Irrespective of the temperatureand genotype, shoot development appeared to be indeterminateand the number of leaves on the main stem of alfalfa was related lin-early to time under constant meristem temperatures (Fig. 1a). Theleaf appearance rate was calculated as the slope of the relationship.By contrast, organ growth (leaf, node and radicle in the dark) allappeared to be determinate, ultimately reaching a maximum organsize. Temperature affected the rate and duration of organ expansion(Fig. 1b). At intermediate temperatures, both effects compensatedfor each other and resulted in unchanged final organ dimensions(i.e. plateau values). However, at extreme growth temperatures(below 10 ◦C and above 30 ◦C), final organ size was significantlyreduced in all genotypes (ANOVA, P < 10−3). For alfalfa, the sizereduction was on average 73% at 5 ◦C and 58% at 35 ◦C, whencompared to the maximum organ size recorded. Maximum organexpansion rates were calculated by fitting a sigmoid model (Eq.(1)) as the derivative at 50% of maximum organ size. No growthor development was observed under the 40 ◦C treatment. At thistemperature, all the plants died within a week.

S. Zaka et al. / Agricultural and Forest Meteorology 232 (2017) 433–442 437

Fig. 2. Comparison of the responses of absolute (a, b, c) and normalized rates (d, e, f) to temperature between different genotypes with respect to leaf appearance in alfalfa( rocesso l fits

r read

3a

iswaStn(EfttCwowTmwaavat−o

a, d), leaf elongation in alfalfa (b, e) and leaf elongation in tall fescue (c, f). Each pf 20 ◦C. Vertical bars indicate 95% confidence intervals. Lines correspond to modeespectively. (For interpretation of the references to colour in this figure legend, the

.2. Effects of temperature and genotype on shoot developmentnd organ growth rates

Shoot development and organ growth rates all displayed a typ-cal bell-shape response to meristem temperature (Fig. 2). In bothpecies, leaf appearance rates (LAR) and leaf elongation rates (LER)ere markedly reduced under high and low temperatures (e.g. an

lmost 6-fold decrease at 5 ◦C as compared to 25 ◦C, Fig. 2a–c; Fig.up. A). Within each species, comparisons of model fits indicatedhat the responses of absolute rates to temperature differed sig-ificantly between genotypes, irrespective of the process studiedStudent’s test and lack of fit test with P-values < 10−3, Sup. Table). Significant intra-specific genetic diversity was thus observedor all processes. Fig. 3 shows the rankings of the genotypes forhe maximum LAR in alfalfa and the maximum LER in alfalfa andall fescue recorded at 27.5 ◦C for tall fescue and 30 ◦C for alfalfa.learly, the genotypic differences in absolute developmental ratesere significant (ANOVA, P < 10−2), but unrelated to the temperate

r Mediterranean origin of the genotype. Much smaller differencesere observed between genotypes for cardinal temperatures (Tmin,

opt and Tmax) than for absolute rates (Fig. 2a–c). In alfalfa, the opti-um temperature for LER ranged from 27.5 ◦C (G3) to 28.7 ◦C (6 10)ith an average of 28 ◦C. In tall fescue, the optimum LER temper-

ture ranged from 26.2 ◦C (Centurion) to 27.7 ◦C (26 10) with anverage of 26.8 ◦C. The Tmax parameter had the smallest range ofariation in the two species (e.g. from 39.3 ◦C to 40.2 ◦C with anverage of 39.8 ◦C for leaf expansion in alfalfa) whereas Tmin hadhe largest (e.g. from −21.0 ◦C to −7.7 ◦C with an average value of

16.1 ◦C for leaf appearance in alfalfa). Standard errors were largern this latter parameter as they were systematically located out-

rate was normalized by the value of the absolute rate at a reference temperaturefor Eq. (2). Blue and red colours refer to temperate and Mediterranean materials,er is referred to the web version of this article.)

side the range of temperatures characterized and deduced fromextrapolations below the last measurement point at around 5 ◦C.

3.3. Effects of temperature and genotype on normalizedtemperature dependencies

In order to facilitate a comparison of the temperature responsesof genotypes with different maximum growth rates, and to enablecomparisons between different physiological processes, all rateswere expressed relative to their absolute rate at 20 ◦C (Fig. 2d–f).Within each species, comparisons of model fits indicated that, con-trary to absolute rates, the responses of normalized LER and LAR didnot differ between the six contrasting genotypes studied (all threetests with P-values > 0.05, except for the distribution of LER residuesin the 8 2 genotype; Sup. Table F). Normalized stem (SER), radicle(RER) and coleoptile elongation rates are further presented in Fig-ure Sup A for the two most studied temperate and Mediterraneangenotypes in each species. Similarly, no significant differences werereported between alfalfa genotypes for IER and SER, and betweentall fescue genotypes for LAR, RER and CER (Sup. Table G). A sin-gle within-species difference was observed, and concerned RER inalfalfa (Barmed, ks and Student’s tests with P-values < 10−2). TheMediterranean genotype displayed a slightly lower radicle elonga-tion rate at 30–35 ◦C in this species.

By contrast, inter-species differences between alfalfa and tallfescue were always significant regarding all developmental pro-cesses (lack-of-fit test, P-values < 10−3). This resulted in lower

cardinal temperatures in tall fescue. For instance, the calculatedTopt values for tall fescue were 27.5 ◦C and 26.4 ◦C for LAR and LER,respectively, as compared to 29.2 and 28.4 ◦C in alfalfa. Hence, tallfescue displayed normalized rates that were higher than alfalfa

438 S. Zaka et al. / Agricultural and Forest M

Fig. 3. Comparison of maximum rates between genotypes for leaf appearance inalfalfa (a), leaf elongation in alfalfa (b) and leaf elongation in tall fescue (c). ValuescVo

at

3e

ttMinoscelatmpp

orrespond to a meristem temperature of 30 ◦C in alfalfa and 27.5 ◦C in tall fescue.ertical bars indicate standard deviations and letters indicate homogeneous groupsf means.

t low temperatures, but lower at optimum and supra-optimumemperatures.

.4. Comparison of normalized temperature dependencies duringarly growth and the vegetative phase in mature plants

Comparisons of the normalized temperature dependencies ofhe different developmental processes are presented in Fig. 4. Dueo the absence of significant differences, the data on temperate and

editerranean genotypes were pooled for each species. Compar-sons of model fits indicated that the responses to temperature oformalized rates differed significantly between most of the devel-pmental processes studied (Sup Table H). These differences wereignificant in both species between LAR, LER, RER and CER whenompared pairwise (except between LER and RER in alfalfa). How-ver, differences in terms of cardinal temperatures were relativelyimited for these processes (e.g. ±2 ◦C and ±2.5 ◦C for Topt; ±1 ◦Cnd ±2 ◦C for Tmax for alfalfa and tall fescue respectively). By con-

rast, normalized internode and stem elongation rates presented

arkedly different response patterns in alfalfa. These two relatedrocesses displayed sharper curves with a narrower range of tem-eratures than the other three processes (Fig. 4a). For SER, Tmin

eteorology 232 (2017) 433–442

and Tmax were respectively 5.0 ◦C and 37.6 ◦C, versus averages of−3.7 ◦C and 39.7 ◦C for LAR. Overall, the temperature responsesthus differed more between processes (e.g. leaf expansion andstem elongation during the vegetative phase of mature plants)than between developmental stages (e.g. seedling and mature plantorgan growth as represented by RER and LER).

4. Discussion

4.1. Evidence for an intra-specific variability of temperaturedependencies is limited

Numerous reports on perennial species have indicated thatMediterranean and temperate genotypes differ in terms of theirseasonality of production (Cooper, 1964; Robson and Jewiss, 1968;Nelson et al., 1978; Volaire and Norton, 2006; Norton et al., 2006.This was also the case in field studies on the two alfalfa (Barmedversus Harpe) and tall fescue (Centurion versus Soni) genotypeswe used during the present study (Gastal et al., 2015). This origi-nally led Cooper (1964) to hypothesize that cultivars from grasslandspecies differ in their responses to temperature. However, ourresults did not support this hypothesis. The response of absolutedevelopmental rates to temperature differed between genotypesfor LAR and LER in alfalfa and tall fescue, but not the correspondingnormalized responses. Differences in the absolute responses couldthus be wholly explained by differences in the maximum ratesof the different genotypes. For a given developmental process, nogenotypic difference persisted between normalized temperaturedependencies, indicating no differences in their cardinal tempera-tures. Although surprising, this finding was consistent with reportson annual crops. Genotypic differences in absolute rates are wellestablished for leaf elongation in tall fescue (Nelson et al., 1977)and corn (Sadok et al., 2007), but no differences were found in thetemperature response of LER between temperate and tropical linesof maize (Parent et al., 2010). Similarly, no QTLs associated withtemperature response parameters were found in mapping popu-lations, indicating an absence of structured genetic variability forthis trait in maize (Sadok et al., 2007; Welcker et al., 2007).

The lack of genotypic variability was also consistent with thegermination rates in response to temperature recently reported inseveral grassland species (Ahmed, 2015). Significant genetic vari-ability was found in the temperature dependency of germinationamong natural populations of perennial ryegrass and tall fescue,but not within selected cultivars. All the genotypes chosen forour study were commercial cultivars, suggesting a theoreticallynarrower genetic variability available for this trait. This commonfeature with many annual crops (Parent and Tardieu, 2012) mayresult from the exclusion by breeders of plants with atypical phe-notypes under the conditions applied during the selection process.By focusing on a limited number of traits related to agronomic per-formance or market needs (e.g. high germination rates), traits ofimportance under particular thermal conditions may have been fil-tered out, even in species with a recent history of selection such asgrassland species.

This discrepancy in the growth patterns of Mediterraneanand temperate cultivars between field and greenhouse conditionsmight be linked to the reproductive status of the plants. Duringour study, all plants were maintained and studied at the vegetativestage. In the field however, successive phases of vegetative growthand reproduction alternate or occur concomitantly, depending onthe species (Lafarge and Durand, 2011). The response of the leaf

extension rate to air temperature has been shown to change dur-ing the reproductive phase in perennial ryegrass (Peacock, 1975;Parsons and Robson, 1980) and tall fescue (Gastal et al., 1992).The shift of the response was found to be related to modifica-

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ions in the morphogenetic status of the shoot meristem during thearliest stages of reproductive development (Parsons and Robson,980; Wang and Engel, 1998; Cookson et al., 2007). Genotypicifferences in the duration of phenological phases (Cooper andcWilliam, 1966; Groves, 1975; Aronson et al., 1992), rather than

n the temperature dependence of developmental processes, mayherefore explain the difference between temperate and Mediter-anean genotypes. Differences in the temperature dependence ofther physiological processes (e.g. photosynthesis, Zaka et al., 2016)ay also be involved.

.2. Some developmental processes display singular temperatureependencies

It has been argued that within a species certain integrated phys-ological processes may display a common short-term response toemperature, independent of the temperature history of the plantParent et al., 2010). This is obviously not the case for physiologicalrocesses that can develop thermal acclimation, such as photosyn-hesis (Hikosaka et al., 2006; Yamori et al., 2014; Zaka et al., 2016)r respiration (Way and Yamori, 2014). But several developmen-al processes, such as expansive growth, shoot organogenesis orermination, have been shown to share a fairly common temper-ture dependency in several species (Warrington and Kanemasu,983; Hammer et al., 2010; Ben-Haj-Salah and Tardieu, 1995;enfield, 2008; Parent et al., 2010; Parent and Tardieu, 2012).his assumption of a coordinated response was not confirmedor all the processes that we characterized in alfalfa and tall fes-ue. Several processes presented very similar patterns of response,lthough there were some significant differences between normal-zed curves (namely LER, LAR, RER and CER in both species), whilethers displayed clear departures with very distinct cardinal tem-eratures (IER and SER in alfalfa). Such differences in sensitivity toemperature have also been highlighted in alfalfa (Allirand, 1998),orghum (Craufurd et al., 1998) and wheat (Porter and Gawith,999). The reasons for differences in the conclusions of thesetudies include the statistical method used, how the short-termesponses were established and the greater number of processesharacterized.

Regarding the statistical method, the lack of fit test we used toompare the temperature dependencies was probably a stricter cri-erion than those employed previously. Parent and Tardieu (2012)ased their conclusions on an approach involving model compar-

son, using the Bayesian Information Criterion to choose between

odels varying in terms of their number of free parameters. Some

f the models they tested made it possible to consider differentesponses between genotypes or processes. The main problemhen applying this approach is that BIC values are highly sen-

ig. 4. Comparison of normalized temperature dependencies between developmental palue of the absolute rate at a reference temperature of 20 ◦C. Data are for temperate and2). CER: coleoptile elongation rate; LAR: leaf appearance rate; LER: leaf elongation rate;

eteorology 232 (2017) 433–442 439

sitive to the number of experimental points, and using it wouldhave required an additional standardization (e.g. data aggregationby temperature class) for which we did not have sufficient dataon each of the studied processes. Furthermore the threshold for aBIC deviation to declare that a difference is significant is somewhatarbitrary. The lack of fit test allowed us to overcome these two limi-tations (Hart, 1997). It proved to be more sensitive in differentiatinga subset of processes for which the comparison of methods was fea-sible (LER/RER in tall fescue or LER/LAR in alfalfa, data not shown),explaining the discrepancy at least in part. A second explanationmay have resulted from the experimental conditions under whichthe developmental responses were established. The time step ofmeasurements only allowed the determination of integrated valuesfor developmental rates under stabilized thermal conditions. Theduration of plant exposure to a given temperature thus lasted forlong periods (several days to weeks), possibly inducing a degree ofacclimation or feedback from integrated plant responses to devel-opmental processes (Atkin et al., 2006; Louarn et al., 2008, 2010).This may have caused departures from a true short-term responsein some processes. However, several of these responses requiretime to be properly determined (e.g. LAR requires several phyl-lochrons, IER requires a delay before node expands, Baldissera et al.,2014) and are generally established under comparable conditions(Craufurd et al., 1998; Yin and Kropff, 1996). Our experimentaldesign provided a trade-off to permit these different characteri-zations on mature plants from both species.

Overall, the consequences of these differences regarding thecomputation of temperature-compensated time were limited forall the processes except coleoptile, shoot and internode elongation(Fig. 5). Under a broad range of climates (typical Mediterranean andtemperate areas at present and under near future projections), thedifferences in the annual number of equivalent days at 20 ◦C com-puted for the two species were small using either of the responses.However, SER, IER and CER induced marked differences (up to theequivalent of two months at 20 ◦C under the colder temperaturescenarios), that ultimately altered the cumulated thermal time esti-mated with a curve common to all processes. This highlights theimportance of considering processes separately when their Tminvalues differ significantly. The recent focus on seemingly coordi-nated Topt should not hide the fact that Tmin is a parameter that isfar more sensitive in the phenology modules of crop models (Rugetet al., 2002). With respect to this particular point, the potentialeffects of the reproductive stage of development on Tmin need tobe assessed in grasses in order to refine our conclusions.

rocesses in alfalfa (a) and tall fescue (b). Each process rate was normalized by the Mediterranean genotypes pooled together. Lines correspond to model fits for Eq.

RER: radicle elongation rate; SER: stem elongation rate.

440 S. Zaka et al. / Agricultural and Forest Meteorology 232 (2017) 433–442

Fig. 5. Difference in temperature-compensated time cumulated annually and calculated when using either of the individual response curves from Fig. 4 or a commonresponse derived from normalized data for all processes aggregated together (All). Comparisons are made for alfalfa (a, c) and tall fescue (b, d) using climate scenarios forc nditiot tile ee

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urrent temperate conditions (a, b, Lusignan site) and projected Mediterranean coime, obtained from the leaf appearance rate response for each species. CER: coleoplongation rate; RER: radicle elongation rate; SER: stem elongation rate.

.3. Consequences for meta-analyses and modelling

Our results confirm the possibility of aggregating data fromifferent genotypes in order to derive the developmental tem-erature dependency of a given species. Furthermore, a commonemperature dependency derived from several processes, includ-ng early seedling growth, yielded thermal time predictions similaro those based solely on the shoot development rate. Both aspectsuggest that a meta-analytical approach, gathering normalizedata from different experiments and genotypes in the literatureParent and Tardieu, 2012), might be useful to determine the tem-erature dependency of herbage species. Meta-analyses could besed to expand the response to a broader range of temperatureshan that originally characterized by a single study and to deter-

ine appropriate optimum temperatures without running newnd costly experiments. Complementary experiments based onhe early seedling growth response may constitute a cost-effectiveption to increase the density of datasets in the extreme ranges ofemperature where data are often scarce.

However, our results also suggest that one should proceed withaution regarding the selection of datasets for a meta-analysis. Notll processes displayed similar temperature responses, and somee.g. SER in alfalfa) resulted in an important bias that affected therediction of temperature-compensated time when compared tohoot development. The selection of datasets should not be driveny data availability alone, and should consider a priori knowl-dge on the temperature-dependency of each process. For instance,hoot growth is a process that is much more frequently charac-erized than leaf growth and the leaf appearance rate in alfalfa

Volenec et al., 1987), but it can cause discrepancies when driv-ng plant development. To date, LAR, LER and the seedling radiclelongation rates have proved fairly similar in their response toemperature in several annual and perennial species, and should

ns (c, d, Avignon, IPCC A1 B scenario). Values are expressed relative to cumulatedlongation rate; IER: internode elongation rate; LAR: leaf appearance rate; LER: leaf

be favoured when selecting datasets used to derive temperatureresponses driving vegetative development. As for shoot elongation(Porter and Gawith, 1999), the germination rates were shown todiffer from the responses of other processes, particularly in nat-ural populations where the proportion of germinating seeds wasdependent on temperature (Ahmed, 2015). Although widely avail-able (Black et al., 2006; Sakanoue, 2010), germination data shouldtherefore be avoided unless the proportions of germinating seedsare reported as being unchanged by temperature.

In crop modelling, a single response to temperature is often usedto drive growth and developmental processes (Ritchie and Otter,1985; Brown et al., 2005; Hammer et al., 2010). In the STICS cropmodel, which can simulate both alfalfa and tall fescue (Ruget et al.,2013), two distinct responses to temperature are used for pheno-logical development and leaf area expansion (Brisson et al., 1998).Our results suggest that it would be worth differentiating sev-eral developmental responses to temperature (at least two), and itwould be efficient to distinguish stem growth from other processes(Allirand, 1998; Porter and Gawith, 1999). This is of particular inter-est when predicting forage production. The leaf to stem ratio ofharvested biomass is a primary factor determining forage qual-ity (Lemaire and Allirand, 1993; Buxton 1996) and, consequently,improving the prediction of this ratio could help to refine modeloutputs in terms of the use-value of the biomass produced.

Acknowledgements

This study received support from the CLIMAGIE project, part ofINRA’s ACCAF metaprogramme, the REFORMA project funded by

the ARIMNet2 call under the ERA-CAPS 7th EU Framework Pro-gramme (grant n◦ 618127) and the MODEXTREME project fundedby the FP7 (grant n◦ 613817). Serge Zaka’s PhD grant was financedby the Poitou-Charentes Regional Council (CPER). Lina Ahmed was

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he recipient of a PhD fellowship from the joint programme France-urdish Region of Iraq. We would like to thank M. Baumont, A.princhard, M. Jubert, M. Langot, N. Moynet and A. Philipponneauor their assistance with the experiments.

ppendix A. Supplementary data

Supplementary data associated with this article can be found, inhe online version, at http://dx.doi.org/10.1016/j.agrformet.2016.0.004.

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