Variability of Phyllochron, Plastochron and Rate of Increase in Height in Photoperiod-Sensitive Sorghum Varieties

Annals of Botany 101: 579-594, 2008 doi:10.1093/aob/mcm327, available online at www.aob.oxfordjournals.org

Variability of Phyllochron, Plastochron and Rate of Increase in Height in Photoperiod-sensitive Sorghum Varieties

B. CLERGET1,*, M. DINGKUHN2 ,E.GOZE´ 2 ,H.F.W.RATTUNDE3 and B. NEY4 1ICRISAT/CIRAD, UPR Agrobiodiversite´ en savanes, BP 320, Bamako, Mali, 2CIRAD, UPR Mode´lisation inte´grative, Avenue Agropolis, 34398 Montpellier Cedex 5, France, 3ICRISAT, BP 320, Bamako, Mali and 4UMR INRA-AgroParisTech Environnement et Grandes Cultures, 78850 Thiverval-Grignon, France

Received: 14 October 2007 Returned for revision: 16 November 2007 Accepted: 4 December 2007 Published electronically: 28 January 2008

† Background and Aims West African sorghum (Sorghum bicolor) varieties are generally highly photoperiod-sensitive, which is a necessary adaptation to the variable onset date of the rainy season and the variable dates of sowing in the savannah zone. Depending on sowing date, plants can produce from 12 to .40 leaves on the main culm, with height varying from 1 m to more than 5 m. The present study aimed to better understand the complex phenology of these variables. † Methods A 2-year series of monthly sowings of three West African sorghum varieties was conducted near Bamako, Mali. Drought stress was avoided by supplemental irrigation. Rate of initiation of primordia at the stem apex was recorded, together with rate of leaf emergence and increase in plant height. † Key Results Leaf initiation and appearance rates (plastochron21 and phyllochron21) were constant for a given sowing date in cases where less than 20 leaves were produced (generally observed with late sowing dates). In contrast, rates were bilinear for early sowing dates, for which plants produced more than 20 leaves. The secondary rates, which occurred from the 20th leaf onwards, were only half of the initial rate. Plastochron and phyllochron showed large variations among sowing dates, and were correlated with the rate of plant height increase. The initial plastochron and phyllochron were positively correlated with soil temperature and negatively correlated with both day length and day-to-day change of day length prevailing at plant emergence, but these factors explained only half of the variation observed. † Conclusions Although they belong to different genetic groups and have different height and photoperiod sensitivity, the three varieties studied exhibited similar response patterns of development rates among phenological phases and seasons, with the local landrace showing the greatest variation due to its longer vegetative phase and longer stem internodes. The possible adaptive advantages in African savannah environments of bilinear development rates and the associated limitation in height increase are discussed.

Key words: Sorghum bicolor, phenology, plastochron, phyllochron, photoperiod, stem growth.

INTRODUCTION over 1 month following the onset of the rainy season. Farmers thus require varieties that flower at the end of the The West African landraces of sorghum (Sorghum bicolor) rainy season regardless of sowing date. The crop’s life cropped under rainfed field conditions during the summer cycle can therefore vary greatly between sowing dates monsoon, from May–June to September–October, are gen- (Clerget et al., 2004). Several studies have been published erally highly photoperiod-sensitive (Grenier et al., 2001). on the determination of the flowering date of West This trait is an adaptation to environments where the African landraces, but the consequences of the variable dur- rainy season is substantially longer than the basic growth ation of the vegetative phase on plant development and cycle of the plant, i.e. the crop duration observed when height dynamics are still poorly documented. The only sub- flowering is not delayed by photoperiod. The effective stantive research on this aspect of sorghum physiology is crop duration expressed in thermal time, which is the time that of Goldsworthy (1970a, b), but is limited to a narrow perceived by the plant, increases as latitude decreases. It range of sowing dates in May. has been observed that flowering of locally adapted land- Wilhelm and McMaster (1995) defined phyllochron as races coincides with the end of the rainy season, which the time elapsing between the visual appearance of two suc- means that varieties adapted to the Sudan and Guinea cessive leaf tips, and the plastochron as the time elapsing savannah zones are late-maturing, with durations to flower- between the production of two successive phytomers at ing longer than 100 d, caused by photoperiod sensitivity the growing point. Rickman and Klepper (1995) reviewed (Curtis, 1968; Andrews, 1973). Due to this mechanism, available information on these processes in grasses. The maturing grains escape pest and disease pressures associ- concept of plastochron and phyllochron is based on the ated with the rainy season, such as moulds, insects and fact that the production rate of new phytomers is often birds. On the other hand, farmers cannot sow their entire found to be nearly constant from seedling stage to flag-leaf crop area at once due to labour limitation and the need expansion when expressed in thermal time units for early weeding, and sowing dates are commonly spread (8Cd, degree-days) in wheat (Gallagher, 1979; Bauer * For correspondence. E-mail [email protected] et al., 1984), barley (Kirby et al., 1982; Ellis and Russell, # The Author 2008. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 580 Clerget et al. — Development and Growth Rates of Sorghum

1984), maize (Birch et al., 1998), sorghum (Muchow and rate of leaf appearance has been demonstrated for wheat Carberry, 1990; Birch et al., 1998; Craufurd et al., 1998) and barley in southern England and Scotland (Kirby and millet (Craufurd and Bidinger, 1988). et al., 1982; Ellis and Russell, 1984; Baker et al., 1990). The corollary of the concept of a constant rate of leaf pro- Leaf appearance rate was thus slow for autumnal sowings duction is that the rate is not continuously affected by the under decreasing days and accelerated for spring sowings. environment. It depends, however, on the sowing date in Slafer et al. (1994b), however, concluded from field experi- wheat and barley (Baker et al., 1980; Ellis and Russell, ments on wheat in southern Australia that phyllochron 1984; Kirby et al., 1985; Miralles et al., 2001), and is there- neither responded to the rate of day-length change nor to fore set early in the life cycle, probably by environment the average, absolute day length. factors at the time of seedling emergence. In sorghum, Lastly, radiation intensity in the field has been found to phyllochron has been described as being independent of be negatively correlated with phyllochron in maize (Birch sowing date by some authors (Muchow and Carberry, et al., 1998) and to a lesser extent in wheat (Rawson, 1990; Craufurd and Qi, 2001), but Vaksmann et al. 1993). Bertero (2001) reported similar findings for quinoa (1998) observed phyllochrons from 45 to 578Cd leaf21 varieties originating from temperate regions, whereas for sowing dates between the end of June and the beginning materials collected in the tropics were only responsive to of August for a sorghum variety of the guinea race, ‘CSM photoperiod (but were insensitive to the rate of day-length 388’, in Bamako, Mali. change). In controlled environments under lower light Temperature has been suggested to be the major factor intensities, Slafer (1995) found no effect of radiation on influencing the phyllochron. Studies conducted under con- phyllochron in wheat. stant temperature have shown that the phyllochron An association between sorghum phenology and height (expressed in8Cd leaf21) increases steadily with tempera- increase has also been reported. Final plant height was ture from 7.5to258C in wheat (Cao and Moss, 1989) observed to be strongly correlated with the duration of the and from 12.5to27.5 8C in barley (Tamaki et al., 2002), vegetative phase for 22 contrasting varieties (Miller et al., while in maize and sorghum the phyllochron remains 1968). This relationship was related to the total number of stable at temperatures from 10–18 to 30 8C, but increases internodes produced, as internodes of late-maturing var- at higher temperature (Tollenaar et al., 1979; Warrington ieties were found to be of constant final length (Bezot, and Kanemasu, 1983; Craufurd et al., 1998). In maize, 1963). Birch et al. (1998) concluded from several field exper- Renewed interest in local agro-biodiversity and current iments that the phyllochron is correlated with the mean efforts of West African breeding programs to develop temperature from emergence to tassel initiation. However, improved, photoperiod-sensitive sorghum varieties various authors have shown that development rate is more (Kouressy et al., 1997) requires a better understanding of closely associated with the soil temperature near the soil the interaction between photoperiod-dependent phenology surface than with the air temperature during early stages (as affected by sowing date and latitude), crop morphology of development (Bonhomme et al., 1984; Jamieson et al., and yield components. This study sought to analyse the 1995; Wilson et al., 1995), and that the temperature of intra- and inter-annual variation of these phenological pro- the apex, where new organs are developed, can significantly cesses for three sorghum genotypes of contrasting phenol- diverge from the air temperature measured at 2 m and is, in ogy through field observations on crops sown on 26 fact, similar to the soil temperature near the surface (Cellier successive monthly sowing dates. et al., 1993; Ben Haj Salah and Tardieu, 1996; Lafarge et al., 1998). Consequently, the daily average soil tempera- MATERIALS AND METHODS ture near the surface is similar to the average temperature of the apex, which in turn permits accurate estimation of plant The three sorghum [Sorghum bicolor (L.) Moench] var- development rate until the onset of the stem elongation. ieties used in this study were ‘CSM 335’ from Mali Thereafter, air temperature is an accurate predictor of devel- (Sorghum Collection of Mali), a tall, traditional, opment rate (Vinocur and Ritchie, 2001). These relation- guinea-race landrace known to be highly photoperiod- ships hold true for plant development itself, i.e. the sensitive; ‘Sariaso 10’, an improved caudatum, less initiation of new leaves by the apex, but less reliably photoperiod-sensitive line bred in Burkina Faso from a predict the rate of leaf appearance, which results from the guinea caudatum cross; and ‘IRAT 174’, a dwarf dual process of apical development and leaf-blade kafir durra, photoperiod-sensitive line also bred in elongation prior to tip appearance (McMaster et al., 2003). Burkina Faso. The ICRISAT Sorghum Breeding program Apart from temperature, day length has been suggested to in Bamako provided seeds of ‘CSM 335’, whereas the be responsible for different rates of leaf appearance other seed came from the CIRAD Genetic Resources Unit observed for different sowing dates. Long photoperiods in Montpellier, France. increase the rate of leaf appearance in wheat and barley Monthly sowings were initiated on 5 July 2000, followed (Masle et al., 1989; Cao and Moss, 1991; Slafer et al., by sowing on or about the 10th day of each successive 1994a) and maize (Warrington and Kanemasu, 1983). In month through to August 2002 at the ICRISAT research contrast, long photoperiods decrease the rate of leaf appear- station in Samanko, Mali (12 8340N, 8 8040W, ance in quinoa (Bertero et al., 2000). In other studies, a 330 m a.s.l.). For sowings from September to May, which strong positive correlation between the rate of day-length required irrigation, the soil was a fine, loamy, Typic change at crop emergence and the subsequently observed Haplaquets (USDA taxonomy; C : L : S 25 : 50 : 25 Clerget et al. — Development and Growth Rates of Sorghum 581 and pHH2O ¼ 4.5) located close to the Niger River, and for (1993) they were 11, 30 and 42 8C; and Lafarge et al. sowings in the wet season from June to August the soil was (1998) reported 11 8C for Tb. In a pre-study conducted on a well-drained, fine, loamy, mixed, isohyperthermic, leaf elongation rates in controlled environments for the Plinthic Paleustalfs (C : L : S 20 : 35 : 55 and pHH2O ¼ three tropical varieties utilized here, cardinal temperatures 5.0). Possible differences in soil fertility between fields of 11, 34 and 52 8C were found (Clerget et al., 2004) and were minimized with fertilizer application (NPK at 128, applied to all calculations in this study. Linearity of 92 and 60 kg ha21 as urea, diammonium phosphate and response was assumed between the cardinal temperatures, KCl). Soil moisture was never limiting due to irrigation with thermal time equal to zero at temperatures below the twice a week in the dry season, keeping the soil near field base or above the maximum (broken-stick model). capacity. Plots consisted of four rows 5 m long, and were sown with 10 grains hill21 at 0.75 0.20 m spacing, and Modelling shoot apex temperature for thermal-time thinned to 3 plants hill21 2 weeks after plant emergence calculations and to 1 plant hill21 at the onset of stem elongation. A ran- domized block design with three replications was used Because systematic errors can result from using wrong during the rainy seasons (July and August 2000, June to reference temperatures for calculations of thermal time, August 2001), and no replication for all other sowing extensive measurements were conducted of soil temperature dates. Plant dissections were done in the three replications at 10 and 2 cm below ground under crop canopies, as well during the first rainy season and in one replication during as air temperature at 2 m, during different seasons. the following seasons, after it had been established that Throughout the experiment, air temperature and relative inter-plot variability was low. Weeding was done by hand humidity at 2 m (sensor HMP45C, Vaisala, Helsinki, and insecticide was applied when infestation required it. Finland), soil temperature at 10 cm depth, solar radiation Leaves of each plant of the two central rows were labelled. (sensor PY, Li-Cor, Lincoln, NE, USA) and rainfall From emergence to panicle initiation, three plants per (tipping bucket by Young, Traverse City, MI, USA) were variety were sampled every week and dissected in order continuously measured at 1-min intervals, and averaged to count the number of leaves initiated on the apex and to or summed on an hourly basis and stored in a data logger measure the stem length. Panicle initiation was recorded (21 X, Campbell Scientific, Shepshed, UK) at a weather when having indisputably occurred, after the initiation of station located not further than 800 m from the experimen- the first branches. The plant stand was little affected by tal fields (Fig. 1A–D). this sampling, since there were several additional plants The temperatures of air at 2 m and soil at 10 cm depth per hill before the onset of the stem elongation and later were also recorded within a plant row using the same only the main culm was harvested, leaving the tillers in methods during specific periods, namely from 12 January place to maintain a continuous plant canopy on the plot. to 14 May 2001, 26 June to 10 December 2001, 16 All three varieties had tillers when their vegetative phase January to 16 April 2002, 13 June to 3 September 2002 was long. Ten plants per variety and per sowing date and 4 February to 14 May 2003. During the 2003 measure- were specifically labelled and the following were recorded ments, the soil temperature at 2 cm depth was also recorded weekly on the main culm: number of leaves already using copper–constantan thermocouples installed at plant emerged from the whorl, number fully exerted (ligulated) emergence and remaining in place until the end of the and senesced (.50 % of the leaf blade area dead), and recording period. plant height at the intersection of the two latest-emerged An additional set of 1-year observations on temperature leaves or at the collar of the flag-leaf. Depending on dynamics of the air at 2 m and the soil at 2 and 10 cm sowing date, the number of observations used to calculate depth under a crop canopy was conducted in 2006–2007 development rate by linear regression varied from 53 to (two replications). Between 8 March 2006 and 7 March 282 for leaf appearance rate and from 16 to 56 for leaf 2007, monthly sowings of sorghum were used to observe initiation rate. these temperatures from 15 to 45 d after emergence. After each observation period, the system was transferred to the next newly sown plot. Calculation of day length and thermal time Apex temperature was assumed to be equal to the soil Daily civil day length (sun 6 8 below the horizon at temperature at 2 cm depth under a crop canopy until jointing, beginning and end of day) was calculated according to because during that period the apex is located near the soil Keisling (1982) based on latitude and calendar date surface. Thereafter, apex temperature was assumed to be (Fig. 1E). Thermal time was calculated on an hourly basis equal to air temperature because stem elongation rapidly using the shoot apex temperature estimated from soil and lifts up the apex. A similar approach was used by Dingkuhn air temperature (see below). Cardinal temperatures were et al. (1995) to characterize the phenology of rice. assumed to be 11, 34 and 52 8C for base, optimal and The observations used to estimate soil temperature at maximum temperatures, respectively. Published values for 2 cm depth are summarized in Fig. 2. Two distinct seasonal cardinal temperatures derived from leaf appearance rates patterns were observed for the relationship between surface- are not uniform, probably due to genetic variation soil and air temperature (Fig. 2A). From December to the between tropical and temperate varieties. According to end of April the daily average temperatures were lower Alagarswamy and Ritchie (1991) Tb, Topt and Tmax were for the soil than for the air, whereas the opposite was true 8, 34 and 52 8C, respectively; according to Hammer et al. from May to November. The underlying diurnal dynamics 582 Clerget et al. — Development and Growth Rates of Sorghum

F IG. 1. Daily climatic conditions at the Samanko station from 1 July 2000 to 31 October 2002. (A) Minimal, maximal and average temperatures, (B) average relative humidity, (C) global radiation, (D) daily rainfall, and (E) civil day length. are shown in Fig. 2(C, D) where a very dry and hot day in day and the night. The diurnal dynamics of the soil temp- April (C) is compared with a humid and cool day in August erature at 2 cm and 10 cm depth were also different, but (D). During the dry season, when plots were generally irri- the difference between their daily averages was always gated, soil temperature was cooler than air temperature, par- smaller than 1 8C, with an annual average difference of ticularly in daytime, possibly due to the cooling effects of only 0.01 8C. evaporation. Conversely, during the rainy season air temp- Finally, the data from the various series recorded at erature was lower than soil temperature throughout the Samanko station being very coherent, an empirical model Clerget et al. — Development and Growth Rates of Sorghum 583

F IG. 2. (A, B) Differences between the daily air (2 m) and soil (10 cm depth) temperature during the year from data recorded in 2001, 2002, 2003 and 2006–2007 (A), and the 10-d common moving average, resulting in a model of the yearly dynamics (B). (C, D) Diurnal variation of air temperature, and soil temperature at 2 and 10 cm depth under a canopy of a 1-month-old sorghum crop for (C) a day in the dry and hot season (10 April 2006) and (D) aday in the rainy season (5 August 2006). was established based on the 10-d moving average to For all calculations of thermal time, modelled soil temp- predict the soil temperature from the air temperature when erature at 10 cm depth was used from crop establishment to not recorded, by subtracting the simulated values D, onset of stem elongation, because the shoot apex is located (Fig 2B; jd ¼ Julian day): at the level of the soil surface during these developmental stages. Thereafter, air temperature was used because the If jd , 15; then D ¼ 137 apex was located well above the soil surface. Figure 3 demonstrates for ‘CSM 335’ that this procedure resulted If 15 jd 32; then D ¼ 137 ½ð287 137Þ= in slightly different dynamics of leaf appearance, as com- ð32 15Þ ð jd 15Þ pared with the conventional method of using air tempera- If 32 jd 80; then D ¼ 287 ture throughout. Importantly, the basic characteristics of phyllochron dynamics, namely their bilinearity (rapid leaf If 80 jd 180; then D ¼ 287 ½ð287 þ 235Þ= appearance rate before jointing and a slow one thereafter), 100ðjd 80Þ were not affected by the choice of model. If 180 , jd 258; then D ¼235 If 258 , jd 325; then D ¼235 þ ½ð15 þ 235Þ= Estimation of rates of development 63ðjd 258Þ Rate of development is defined here as the reciprocal of If 325 , jd 350; then D ¼15 þ½ð137 þ 15Þ= the thermal time elapsing between two development events, 25ðjd 325Þ such as initiation, appearance or ligule emergence of two If jd . 350; then D ¼ 137 successive leaves on the main culm. This can also be expressed as the slope of leaf number vs. thermal time on ð1Þ linear portions of the relationship. As shown in the example in Fig. 4, dynamics of leaf appearance were generally linear, but sometimes showed an abrupt change in Figure 2B shows that the accuracy of the prediction of slope in mid-season. This was interpreted as a bilinear surface-soil temperature from air temperature was low behaviour, consisting of an initial and a secondary, slower when applied on a daily basis, but satisfactory on a development rate. monthly basis, which is the minimum duration of the vege- Rates of leaf development were fitted to either linear or tative phase observed for sorghum under field conditions. bilinear dynamics using a segmented model. Observed 584 Clerget et al. — Development and Growth Rates of Sorghum

F IG. 3. Differences in the relationship between the number of leaves visible on the main stem and thermal time, depending on the calculation of thermal time. Thermal time was either calculated with the air temperature (2 m) or with the estimated apex temperature. Apex temperature was presumed to be equal to soil temperature before jointing and to air temperature during jointing. Data is presented for the variety ‘CSM 335’ and sowing dates with contrasting air–soil temperature differences in February (soil colder than air), May (similar) and August (soil warmer than air) 2001.

leaf number (LN; initiated, emerged, ligulated or senesced) where a is the number of leaves at emergence, b1 and b2 are was regressed against the elapsed thermal time from emer- the initial and secondary rates of development, respectively, gence (TFE) using one of the following equations: and TS1 and TS2 are the thermal time when either the change of rate occurred or the development terminated. The intercept was set to a ¼ 1 when modelling the number of emerged leaves, because the ﬁrst leaf exerts LN ¼ a þ½b minðTFE, TS1Þ 1 immediately from the coleoptile at emergence under tropi- LN ¼ a þ½b1 minðTFE, TS1Þþ cal conditions. When modelling the number of initiated ¼ fb2 min½TS2 TS1; maxð0; TFE TS1Þg leaves, it was set to a 5, the number of leaves already

F IG. 4. Relationship between the number of leaves visible on the main stem and the thermal time for 26 sowing dates between July 2000 and August 2002, for three sorghum varieties (‘CSM 335’, ‘Sariaso 10’ and ‘IRAT 174’). Lines were fitted by regression analysis; the horizontal, dotted line marks the 20th. For clarity, different symbols are used for each monthly sowing date. Clerget et al. — Development and Growth Rates of Sorghum 585 pre-formed in the embryo at emergence, as estimated for and Chandra, 1998), meaning that after 10 d plants have sorghum (Paulson, 1969; Muchow and Carberry, 1990). perceived their environment and triggered their response. Parameters and their confidence intervals were iteratively estimated using the procedure NLIN of SAS (2004). The choice between the linear and bilinear models was made Estimation of height increase rates through a stepwise process. First, both models were A similar comparison of models was performed to calcu- applied to each sowing date. The linear model was selected late the segmented regression of plant height (Ht) against either when the bilinear model did not converge due to non- thermal time (SumT), using two models in order to determination of certain parameters, or when the reduction include two or three segments. The equations were: of the sum of squared errors (SSE) resulting from the use of the bilinear model was non-significant. This was tested with Ht ¼½b minðSumT, ST Þ þ fb min½ST ST ; an F-value, calculated as 1 1 2 2 1 maxðSumT ST1; 0Þg ð3Þ

Fobs ¼½ðSSElin SSEbilinÞ=2=½SSEbilin=ðn pbilinÞ ð2Þ Ht ¼ [b1 minðSumT, ST1Þ] þfb2 min½ST2 ST1;

maxðSumT ST1; 0Þg þ fb3 min½ST3 ST2; with SSElin and SSEbilin being the SSE of the linear and bilinear regression models, respectively, n is the number maxðSumT ST2; 0Þg of observations, and plin and pbilin are the number of parameters of the linear and bilinear models (Seber and where b1, b2 and b3 are the slopes, and ST1,ST2 and ST3 are Wild, 1989). the values of SumT at the inflection or ending points. The linear model was accepted when the probability of Parameters were iteratively estimated with the procedure . exceeding F(n 2 pbilin, n 2 plin) was greater than 0 01. NLIN of SAS (2004) and one of the models was retained, This procedure was applied to the observations on based on an F-test at P ¼ 0.01 as described above. Rate initiated, emerged, ligulated and senesced leaves indepen- of height increase, thermal time at panicle initiation, and dently. Phyllochron and plastochron were calculated as inflection points for leaf appearance and height increase the reciprocal of the slope coefficients for leaf initiation were plotted against sowing dates. Linear-regression ana- and appearance, respectively. lyses of height increase rate vs. phyllochron were calculated Correlations between the number of initiated and using the procedure NLIN of SAS (2004). emerged leaves in the dissected samples, which were also bilinear, were calculated with the same procedure. For comparisons of leaf production rates among varieties RESULTS and among sowing dates, only the initial, linear portions of Rates of leaf appearance, initiation and senescence the dynamics (initial phyllochron or plastochron) were used, regardless of the linear or bilinear nature of the The total number of leaves produced per plant (mean + 5% pattern. As the number of leaves at emergence is equal to C.I.) varied between a minimum of 12.0(+0.5), 14.1 1, an intercept-less regression model was fitted on the (+0.6) and 11.5(+0.4) and a maximum of 41.8(+2.0), number of leaves minus 1. Standard errors were estimated 28.8(+1.5) and 38.8(+1.3) for ‘CSM 335’, ‘Sariaso using the available replicates as independent subjects in a 10’ and ‘IRAT 174’, respectively (Fig. 4). Rates of leaf random slope model (Verbeke and Molenberghs, 1997). appearance were constant for the initial 20 leaves, as indi- As the variance of the residuals was roughly proportional cated by the linear slopes when plotting leaf number vs. to the estimated number of leaves, a generalized linear thermal time. However, rates decreased abruptly in ‘CSM mixed model was fitted, using SAS/STAT software (2004) 335’ and ‘Sariaso 10’ and sometimes in ‘IRAT 174’ after and the Glimmix macro (Littell et al., 1996). As this com- the appearance of about 20 leaves, suggesting a bilinear parison was applicable only to the initial slopes, the second- curve of leaf number vs. thermal time. We henceforth ary phyllochrons were compared using the standard errors refer to an initial (short) and secondary (long) phyllochron, estimated with the SAS NLIN procedure. the latter apparently occurring only when a large number of Lastly, in order to explain seasonal variations in initial leaves is produced. The initial phyllochron, exhibited until phyllochron, this was regressed against the five environ- the appearance of the 20th leaf, varied among sowing mental variables observed at plant emergence, using a step- dates but was nearly identical for all three varieties wise multiple linear-regression model. The explanatory (means + 5% C.I.: 45.4 + 0.3, 46.9 + 0.4 and 46.6 + 0.4 variables, whose daily values were averaged for a 10-d for ‘CSM 335’, ‘Sariaso 10’ and ‘IRAT 174’, respectively] period to reduce noise, were daily temperature, relative and averaged 46.38Cd leaf21 across dates. The varieties did, humidity and global sun radiation averages, astronomical however, exhibit differences for mean phyllochron values day length and its day-to-day rate of change. The under- for leaves of rank greater than 20, with that of ‘CSM lying hypothesis was thus that the phyllochron is set by 335’ (89.08Cd leaf21) twice that of its initial value, environmental conditions prevailing at crop establishment. whereas ‘Sariaso 10’ (84.48Cd leaf21) and ‘IRAT 174’ The choice of the initial 10 d as a reference period also (63.28Cd leaf21) exhibited smaller increases. Whenever a had a physiological basis, because it is the minimum dur- change of phyllochron occurred, it was between the esti- ation to panicle initiation (Ellis et al., 1997; Alagarswamy mated appearance of the 16th and 22th leaf for ‘CSM 586 Clerget et al. — Development and Growth Rates of Sorghum

335’, 15th and 21st for ‘Sariaso 10’, and 13th and 23rd for similar to Figs 1 and 2 (data not shown). The rate of leaf ‘IRAT 174’. However, when the total number of leaves pro- senescence was bilinear when more than about 20 leaves duced on the culm was below 25, the phyllochron remained were produced, and the rate changed between the 10th constant until flag-leaf appearance. and the 15th leaf to appear. Patterns of leaf initiation (Fig. 5) resembled those of leaf appearance. Where the rate of leaf appearance was constant throughout the life cycle, this was also true for the rate of Relationships among development rates leaf initiation, and where patterns were bilinear, this gener- Three main patterns of relationship were observed among ally applied to both variables alike. The average value of the dynamics of leaf-initiation, appearance, ligule exertion the initial plastochron (before inflection) was the same for and leaf senescence over a year-round cycle of monthly the three varieties (38.6 + 1.38Cd leaf21,39.0 + 1.4 and sowings for ‘CSM 335’ (Fig. 6). The first pattern, rep- 38.2 + 1.4 for ‘CSM 335’, ‘Sariaso 10’ and ‘IRAT 174’, resented by a February sowing, exhibited very large total respectively). Whenever a bilinear pattern of leaf initiation leaf number (39) and bilinear development rates, whereby occurred, the plastochron roughly doubled, averaging 92.9 secondary rates were nearly identical for initiation, appear- and 80.68Cd leaf21 for ‘CSM 335’ and ‘IRAT 174’ ance, ligule exertion and senescence. The secondary phase across all dates. The secondary plastochron, where it spanned very contrasting climatic conditions, with April occurred, was similar to the secondary phyllochron and May being hot and dry, June transitory, and July and (Figs 6 and 7). Changes in the rate of leaf initiation August fully in the rainy season with lower temperatures (plastochron21) occurred between the initiation of the and high humidity (Fig. 1). The inflections of these four 20th and 25th leaf. When the total number of leaves did dynamics occurred at about the same thermal time after not exceed 25, the rate of leaf initiation stayed constant sowing (approx. 6008Cd). At that time, an average of until flag-leaf appearance. 21.9 leaves had been initiated, 15.9 had emerged and 6.0 The rate of leaf senescence (example data shown for senesced. (But leaf appearance rate sometimes changed ‘CSM 335’ in Fig. 6) also exhibited either linear or bilinear later than leaf initiation rate on other sowing dates.) After kinetics. Similar to leaf initiation and appearance, leaf inflection, the similar secondary rates for the four develop- senescence kinetics depended on the sowing date and the ment variables resulted in a stable architecture of the whorl total number of leaves produced, resulting in patterns with six leaves growing inside the sheaths and three

F IG. 5. Relationship between the cumulative number of leaves produced by the apical meristem and thermal time for 26 sowing dates between July 2000 and August 2002, for three sorghum varieties (‘CSM 335’, ‘Sariaso 10’ and ‘IRAT 174’). Lines were ﬁtted by regression analysis; the horizontal, dotted line marks the 20th. For clarity, different symbols are used for each monthly sowing date. Clerget et al. — Development and Growth Rates of Sorghum 587

F IG. 6. Relationships between the cumulative number of leaves initiated, emerged, ligulated and senesced on the main stem and the thermal time from emergence for February, July and September 2001 sowings of ‘CSM 335’. Time of the onset of jointing (Jt), panicle initiation (PI) and fully expanded ﬂag-leaf stage (F-L) are indicated. Error bars indicate the 95% conﬁdence interval of each mean value of the number of emerged leaves.

four development variables remained linear throughout the crop’s life cycle. These three patterns were observed on ‘CSM 335’ and ‘Sariaso 10’, but less clearly on ‘IRAT 174’. The relationship between the number of initiated and emerged leaves was very tight and independent of variety and sowing date across all developmental stages (Fig. 7). This relationship was clearly bilinear:

NFA ¼1 44 þ½0 75 minðNFI; 21 35Þ þ ½1 00 maxð0; NFI 21 35Þ

with NFI and NFA the numbers of leaves initiated and emerged, respectively. Consequently, leaf appearance rate was lower than initiation rate until 21.4 leaves were initiated, resulting in F IG. 7. Relationship between the number of initiated vs emerged leaves in a slope smaller than 1 (Fig. 7). During the second phase, the 1512 dissected samples (three varieties and 26 monthly sowing dates). both developmental rates were equal (slope ¼ 1). The different symbols indicate different frequencies of similar observations. The 1 : 1 line and co-ordinates of the inﬂection point are plotted.

Effects of sowing date on development rates emerged, elongating leaves constituting the whorl. The internodes above the three leaves that had the most-recent Initial phyllochron varied between 40 and 658Cd for all fully expanded leaf sheaths elongated, causing the leaf three varieties and showed distinct seasonal patterns sheaths to telescope out from one another. This architec- (Fig. 8). The initial phyllochron had two annual minima tural steady state was observed for a period up to 3 (January and July) and two annual maxima (May and months, depending on sowing date. It was typical of all September). From the random slope model analysis, the sowings between January and the beginning of June, all effects of sowing date (differences among months) were of which produced more than 25 leaves (Figs 4 and 5). significant (P , 0.0001, Table 1), but there was also an The second pattern, represented in Fig. 6 by the July effect of the year (P ¼ 0.0008). Slopes were not signifi- sowing, was observed when the total leaf number was cantly affected by variety nor by the interactions of between 20 and 30. The plastochron showed no inflection variety sowing date and variety year (P . 0.05). and was thus constant until panicle initiation, whereas the As the initial phyllochron for each sowing date remained dynamics of tip and ligule appearance were bilinear constant until the appearance of the flag leaf or onset of the (mean inflection when 16.7 leaves had emerged). The secondary phyllochron, environmental conditions at the dynamics of the senescent leaf number was also bilinear time of plant emergence appeared to determine the initial or curvilinear, but the inflection point could not be clearly phyllochron. Significant positive correlations were observed identified. in the paired-correlations matrix between initial phyllo- The third pattern, represented by the September sowing, chron and soil temperature and global radiation during the was observed when less than 20 leaves were produced 10 d following emergence, but not with relative humidity, on the main culm. In such cases, the dynamics of all photoperiod or rate of change of day length. The same 588 Clerget et al. — Development and Growth Rates of Sorghum

F IG. 8. Initial phyllochron values from emergence and secondary phyllochron values after rate change plotted against calendar date of sowing for observations between July 2000 and August 2002. Error bars indicate the asymptotic 95% conﬁdence interval.

TABLE 1. Analysis of covariance on repeated measurements decreased from 120 to 608Cd from the January to the to test effects of variety, and month and year of sowing on the July sowing date (Fig. 8A). It thus decreased as the duration initial rates of leaf appearance (slope of regression in of the vegetative phase and the total leaf number decreased thermal time). Interactions between factors and thermal time (Fig. 4), and then disappeared from July sowings onwards indicate effects on slope, while single factors indicate effects when crop duration and total leaf number were small. on the intercept The ratio of the secondary over the initial phyllochron was between 1.6 and 2.5 for ‘CSM 335’ but the large d.f. scatter of the data did not allow a seasonal trend to be ident- Source Num Den FPified (data not shown). In addition for ‘CSM 335’, the phenological stage at which the phyllochron changed from its Thermal time 1 24.9 33166 ,0.0001 initial to its secondary rate varied among sowing dates, Thermal time variety 2 24.92.0ns with the inflection point corresponding to the appearance Thermal time sowing month 11 24.848.9 ,0.0001 of the 15th to 16th leaf for January–February sowings Thermal time year/sowing month 14 24.96.9 ,0.0001 Thermal time variety sowing 22 24.71.3ns and increasing to the 18th to 19th leaf for the May–June month sowings (data not shown). Thermal time variety year/ 28 24.82.2ns sowing month Effects of sowing dates on increase in plant height d.f.: degree of freedom, Num: numerator and Den: denominator. Final plant height varied two- to three-fold among analysis conducted for individual varieties identified the sowing dates for ‘CSM 335’ (1.6–4.7 m), ‘Sariaso 10’ same predictor variables but at a lower level of probability (1.1–2.4 m) and ‘IRAT 174’ (0.6–1.9 m; Fig. 9). The (data not shown). height of the whorl at which panicle initiation occurred However, a stepwise multiple linear regression of the varied from ,25 cm up to 3 m (in the latter case, jointing initial phyllochron against the same five mean environ- was more than half completed). The rate of increase in mental variables at emergence showed that a combination plant height exhibited seasonal differences, with the of three of them (soil temperature, photoperiod and daily highest rates observed for sowings in July and September change of the photoperiod) could explain 40–50% of the for ‘CSM 335’ and ‘Sariaso 10’ (Fig. 10). Seasonal differ- observed variability of the initial phyllochron of the three ences in rate of increase in height were greater in absolute varieties, individually or together (Table 2). Photoperiod and relative terms for ‘CSM 335’, a tall variety having a and its daily rate of change were both significantly corre- maximal internode length of 25 cm, than for ‘Sariaso 10’, lated with soil temperature in the correlation matrix, but a semi-dwarf (16 cm) and ‘IRAT 174’, a dwarf (8 cm). not with global radiation or relative humidity. The phyllo- Although rates of increase in height were generally higher chron was thus significantly increased by higher soil temp- for sowing dates falling into the wet season (June– erature at emergence and decreased by longer photoperiods September) than the dry season, rates for ‘CSM 335’ and or increasing day length. ‘Sariaso 10’ for August sowings were low in both years The secondary phyllochron showed a strong response to for unknown reasons. sowing date for ‘CSM 335’ (Fig. 8A) but not for the There was a significant, negative relationship between the other varieties, where large error terms and insufficient rate of increase in height and the plastochron or the phyllo- data points made a seasonal trend analysis impossible chron during jointing for ‘CSM 335’ (R2 ¼ 0.39 or 0.28, (Fig. 8B, C). In ‘CSM 335’, the secondary phyllochron P , 0.001 or 0.01) and ‘Sariaso 10’ (R2 ¼ 0.37 or 0.22, Clerget et al. — Development and Growth Rates of Sorghum 589

TABLE 2. Multiple, linear-regression parameters and ﬁts for the initial phyllochron vs three climatic parameters at emergence selected through the stepwise process, for the three varieties individually and combined (parameters global radiation and relative air humidity were rejected)

Coefﬁcients

Top-soil temperature (8C) Day length (h) Change of day length (s d21) Model Intercept (8Cd) value Value Partial P Value Partial P Value Partial P Adjusted R2 P

‘CSM 335’ 114.92.15 2 1025 29.59 4 1025 20.11 9 1024 0.51 3 1024 ‘Sariaso 10’ 99.72.23 1 1024 28.45 1 1023 20.13 1 1023 0.40 2 1023 ‘IRAT 174’ 103.82.05 3 1024 28.42 9 1024 20.07 3 1022 0.39 3 1023 Combined 106.12.14 ,1 1028 28.82 ,1 1028 20.11 ,1 1028 0.45 ,1 1028

P , 0.001 or 0.05). The initiation of stem elongation, or DISCUSSION jointing, approximately coincided with panicle initiation Dynamics of leaf production and appearance for the August-to-October sowing dates (Fig. 11). For January through to July sowing dates, a period that includes This study demonstrated the existence of bilinear dynamics the normal dates when farmers sow sorghum (late-May to for leaf initiation and appearance in highly photoperiod- early July), the onset of jointing occurred earlier than sensitive sorghums from West Africa. Previous obser- panicle initiation and was associated with the phyllochron vations of the rates of leaf appearance in sorghum have inﬂection point whenever it occurred (‘CSM 335’ and not reported bilinear kinetics (Muchow and Carberry, ‘Sariaso 10’ only). 1990; Ritchie et al., 1998; Craufurd et al., 1999; Craufurd

F IG. 9. Weekly observations of plant height plotted against thermal time from emergence, for 26 sowing dates of three varieties. Lines were ﬁtted using a linear-segmented model, with plant height at panicle initiation indicated by a solid square. For clarity, different symbols are used for each monthly sowing date. 590 Clerget et al. — Development and Growth Rates of Sorghum

F IG. 10. Relationships between the rate of plant height growth during jointing and the calendar date of sowing. Error bars indicate the asymptotic 95% confidence interval. and Qi, 2001). This may be due to prior work being con- observed in wheat and barley (Baker et al., 1986; Hay ducted with less-photoperiod-sensitive germplasm or in and Delećolle, 1989; Cao and Moss, 1991; Calderini environments in which total leaf number did not exceed et al., 1996; Miralles et al., 2001; Gonza´lez et al., 2002; 25, while as many as 38 and 41 leaves where produced Abeledo et al., 2004). by ‘IRAT 174’ and ‘CSM 335’, respectively, due to their The mean initial phyllochron observed in this study was strong photoperiod-sensitivity that extended pre-floral 468Cd leaf21, or about 3 d, and the mean initial plastochron development to up to 8 months. Bilinear leaf appearance was 368Cd leaf21, or about 2 d, averaged over all three var- dynamics have been observed in wheat (Baker et al., ieties and sowing dates. These values are similar to pre- 1986; Hay and Delećolle, 1989; Cao and Moss, 1991; viously reported values for sorghum. Ritchie et al. (1998) Gonza´lez et al., 2002), barley (Miralles et al., 2001; observed the phyllochron to be 498Cd leaf21. The phyllo- Abeledo et al., 2004), rice (Tivet, 2000; Itoh et al., 2001) chrons (60.9 and 69.08Cd leaf21) and plastochrons (46.9 and maize (Zur et al., 1989; although not recognized by and 40.38Cd leaf21) reported by Birch et al. (1990) and this author). The inflection point observed in photoperiod- Muchow and Carberry (1990), respectively, were higher; sensitive sorghums in this study occurred at a much however, their calculations were used a base temperature higher leaf rank (15–20) as compared with wheat and of 8 and 7 8C, compared to 11 8C in this study, which barley (5–7; Baker et al., 1986; Hay and Delećolle, 1989; was based on observations on West African sorghums Cao and Moss, 1991; Calderini et al., 1996; Miralles (Lafarge and Tardieu, 2002). Re-estimation of the phyllo- et al., 2001; Gonza´lez et al., 2002; Abeledo et al., 2004). chron and plastochron in this study using a base temperature The secondary phyllochron and plastochron in this study of 7 8C gave a phyllochron of 558Cd leaf21 and a plasto- were 1.2–2.5 times longer than the initial phyllochron and chron of 448Cd leaf21, closer to the values reported by plastochron, depending on the sowing date (Fig. 8A). A Birch et al. (1990) and Muchow and Carberry (1990). similar range of 1.2–2.1 times increase over initial phyllo- A consequence of the initial plastochron always being chron rates, depending on variety and sowing dates, was shorter than the initial phyllochron is that the number of

F IG. 11. Thermal time from sowing to the beginning of jointing, panicle initiation and the inflection point of the rate of leaf initiation, as a function of calendar date of sowing; for main culms on three sorghum varieties. Error bars indicate the asymptotic 95% confidence interval of the onset of jointing. Clerget et al. — Development and Growth Rates of Sorghum 591 leaves growing inside the leaf sheaths increases from four at the elongating leaves and the elongating internodes. emergence to about six when the initiation and appearance Alternatively, competition among growth processes for rates changed (inflection point). This observation is resources such as assimilates, for example triggered by common for cereals (Rickman and Klepper, 1995; the onset of stem elongation, might also explain the Vaksmann et al., 1998), except for rice where the plasto- observed synchronicity of rate changes. Whether develop- chron and phyllochron are equal (Nemoto et al., 1995). It ment-related signalling processes, competition effects or has been suggested that the phyllochron is necessarily both combined [for example, sugar-availability-based longer than the plastochron because leaf appearance signals; Black et al. (1995); Roitsch et al. (2000)] are at requires the tip of the elongating leaf to travel the length work here could only be evaluated with specifically of the enclosing leaf sheath. If the elongation rate is sup- designed experiments. posed to be constant for subsequently developing leaves, The tight relationship observed between the number of the increasing distance (length of enclosing sheath) would leaves initiated and the number of leaves emerged for a lead to increasing delays in leaf-tip appearance (Skinner given variety, across sowing dates and across varieties, and Nelson, 1995; Fournier and Andrieu, 1998). agrees with previous observations on wheat (Kirby, 1990) A major phenological consequence of the variable phyl- and maize (Padilla and Otegui, 2005). In maize, with a lochron during stem elongation of photoperiod-sensitive maximal number of 25 leaves produced, the relationship sorghums (caused by facultative linear or bilinear dynamics was found to be linear and had a slope of 0.63, smaller and strong seasonal effects on the secondary phyllochron) is than the initial slope of 0.75 calculated here for sorghum. that the time elapsing from panicle initiation to flag-leaf Consequently, the difference between the number of appearance is highly variable. The photoperiod-sensitive leaves emerged and initiated increases more rapidly in variety ‘CSM 335’, when sown in May, exhibited a second- maize than in sorghum. As indicated by the uniform beha- ary phyllochron of 658Cd leaf21, versus 428Cd leaf21 for viour of the three sorghum varieties studied here (Fig. 6), June sowing. In both cases, six leaves that had yet to appear which belong to different genetic groups and represent were present at panicle initiation. The duration from panicle different plant types, the relationship between leaf initiation initiation to flag-leaf appearance of the May sowing was and appearance dynamics is a characteristic of the species. thus extended by 1388Cd [¼ 6 (65 – 42)] or about 9 d, It is therefore possible to predict leaf and panicle initiation assuming a daily average temperature of 26 8C. This, dates from observations on leaf appearance. together with the increased number of leaves elongating The time at which cereals begin to joint has often been within the sheaths, can combine to prolong the period reported to coincide with panicle initiation (House, 1985; between panicle initiation and flag-leaf appearance from Alagarswamy and Ritchie, 1991; Ritchie et al., 1998). 2008Cd for an August sowing to 5008Cd for a June sowing However, stem elongation can begin before panicle (Clerget et al., 2004). initiation in late-maturing varieties of sorghum and pearl millet (Lane, 1963; Goldsworthy, 1970b; Lambert, 1983). Both cases were observed in this study, depending on the Apparent co-ordination among growth and development variety and sowing date. Panicle initiation and onset of processes jointing coincided for sowings between August and This study demonstrated that when leaf production rates October for all genotypes. In contrast, earlier sowing change from the initial to the secondary rate (associated dates generally resulted in panicle initiation occurring sig- with situations where total leaf number is greater than nificantly later than onset of jointing (by up to 15 phyllo- 25), the rate of leaf appearance and leaf senescence chrons), indicating that initiation of flowering is not change at about the same time. This synchronicity occurred required for the initiation of stem elongation in sorghum. across a wide range of sowing dates, although the phenolo- Whenever these two events did not coincide, stems began gical stage varied (18 and 25 leaves initiated). In fact, leaf elongating at the time of the plastochron and phyllochron initiation is a developmental process, whereas leaf appear- inflection points. ance results from a combination of two processes, develop- For wheat, a synchronization of the phyllochron inflec- ment and growth inside the enclosing sheath (McMaster tion point with double-ridge formation, assumed to occur et al., 2003). The observation of nearly simultaneous just prior to the appearance of the fifth leaf below the flag changes of both initiation and appearance rates suggests leaf, was suggested by Baker et al. (1986) and supported that the rate of development (cell division and differen- by Hay and Delećolle (1989) and Cao and Moss (1991). tiation processes in the apex) and the rate of elongation (a Gonza´lez et al. (2002), however, found no association process happening at some distance from the apex) were between the change of phyllochron and any specific devel- simultaneously altered at the inflection point. The height opmental stage. Likewise, Miralles et al. (2001) found no increase of the stem, driven by the simultaneous elongation relationship between changes of the rate of leaf appearance of the internodes of the last three phytomers carrying fully and final leaf number or any particular development stage in expanded leaves, was also altered in plants showing a sec- barley. The phyllochron was observed to change after ondary phyllochron, as compared with plants that did not panicle initiation in rice by Katayama (1951, cited by and produced less than 20 leaves. Tivet, 2000) and Baker et al. (1990), whereas Nemoto It therefore seems that the change from primary (rapid) to and Yamazaki (1993, cited by Tivet, 2000) suggested that secondary (slower) development rates is a co-ordinated and the change was associated with the beginning of internode regulated event, involving different organs such as the apex, elongation. 592 Clerget et al. — Development and Growth Rates of Sorghum

Environment effects on development rates 2000). Therefore, a longer phyllochron delays the onset of elongation of each successive internode. Since these The significant variation of development rates among delays increase the time available for the growth of each sowing dates, as observed in this study, contradicts internode but do not affect its final length (Bezot, 1963), reports by Muchow and Carberry (1990) and Craufurd it is probable that their elongation rate is reduced propor- and Qi (2001), but agrees with Vaksmann et al. (1998). tionally, and that elongation of the three internodes in the Various relationships of development rates with sowing zone of elongation occurs continuously at this reduced rate. dates were observed in wheat and barley (Baker et al., 1980; Kirby et al., 1985; Cao and Moss, 1991; Rickman and Klepper, 1995). Where the phyllochron was found to Patterns of development rates vs. adaptation to environment be affected by sowing date, the causal factor was not clearly identified, although correlations were found with The high variability of crop duration in photoperiod- temperature (Cao and Moss, 1989; Tamaki et al., 2002), sensitive sorghums in response to sowing date has been thermo-photoperiodic index (Cao and Moss, 1991), day described as an important adaptive mechanism that helps length (Warrington and Kanemasu, 1983; Masle et al., match growth duration with the period of moisture avail- 1989; Cao and Moss, 1991; Slafer et al., 1994b; Bertero ability or, more specifically, synchronizes flowering with et al., 2000), the rate of change of day length at emergence the probable end of the rainy season (Bunting and Curtis, (Kirby et al., 1982; Ellis and Russell, 1984; Baker et al., 1968; Curtis, 1968; Andrews, 1973; Kassoum and 1990) and radiation intensity (Rawson, 1993; Birch et al., Andrew 1975; Kouressy et al., 1997; Vaksmann et al., 1998; Bertero, 2001). The significant, positive correlation 1998; Clerget et al., 2004). This study shows that sowing of the initial phyllochron with soil temperature at plant a photoperiod-sensitive sorghum variety earlier in the emergence found in this study (Table 2) is in agreement year not only extends its growth cycle, but also reduces with some of the reports cited above. This is also true for its rate of development and height increase during jointing. the observed, negative correlation between the initial phyl- The consequences of these reduced rates of development lochron and day length and day-to-day change in day and growth for plant architecture may indeed constitute length. On the other hand, the absence of a correlation of adaptive advantages. phyllochron with solar radiation as reported here contrasts One consequence of reduced rates of leaf formation with previous reports of negative correlations, mainly in during jointing is that internode production is reduced to maize and quinoa. However, the experimental conditions the same extent. In this study, this translated into reduced were different, the present work being based on high plant height because final internode length was fairly solar global-radiation levels (18.0–24.6MJm22 d21), stable among environments (data not shown). The longer, whereas studies indicating negative effects of solar radi- secondary phyllochron, which was particularly long when ation on phyllochron used lower ranges of light levels the crop was sown early and thus had a long crop duration (2.2–19.2MJm22 d21 in Birch et al., 1998, and 8.6– (Fig. 11), may thus serve to prevent excessive plant height 18.6MJm22 d21 in Bertero, 2001). Although our study under conditions of long crop duration. Even with these provides strong evidence for seasonal effects on the initial reduced, secondary development rates, photoperiod- phyllochron, it cannot advance solid evidence on the sensitive sorghums commonly attain plant heights of 5 m environmental signals causing them. It is quite likely, or more when sown early (as for ‘CSM 335’), which may however, that whatever environmental signal is responsible approach the limits of mechanical stability for an annual it sets the phyllochron at an early stage of plant develop- cereal crop. ment, because the initial phyllochron is remarkably con- Furthermore, the stem of tall, tropical sorghum varieties b stant. If standard climatic variables such as solar is the heaviest organ of the plant (Goldsworthy, 1970 ), radiation, temperature or day length during seedling stage exerting a high demand for photosynthates and mineral indeed constitute the signal, experiments under controlled nutrients. Reduction of the rates of internode and leaf devel- conditions could probably provide better evidence than opment probably results in a concomitant reduction in the field experiments, in which these factors vary not only demand for resources for vegetative growth under day- among seasons but also between and within days. length conditions unfavourable to flowering, as compared with less photoperiod-sensitive varieties or species. Maize, for example, exhibits a single and comparatively high rate of development (Warrington and Kanemasu, Environment effects on rate of increase in plant height 1983). Photoperiod-sensitive West African sorghums are The rate of increase in plant height during jointing varied considered as robust crops that are able to grow and among sowing dates (Fig. 10) and was correlated with the produce under conditions of poor soil fertility (Giraudy plastochron and the phyllochron during jointing. This et al., 1997). This characteristic might in part be attributable relationship is probably the result of physiological to the phenological adaptations described here. The co-ordination between the dynamics of internode response to photoperiod expressed in this germplasm there- elongation and leaf appearance. It has been reported that fore covers an ensemble of phenological processes, includ- the elongation of the ith internode is triggered by the emer- ing not only the well-known response of flowering date gence of the collar of the ith leaf from the previous leaf’s (considered as a mechanism for temporal escape), but sheath enclosing it, and growth of this ith leaf (blade and also an intricate regulation of development and the sheath) ends at the same time (Fournier and Andrieu, growth processes associated with it. The latter may have Clerget et al. — Development and Growth Rates of Sorghum 593 adaptive functions that have so far escaped ecophysiologi- Cao W, Moss DN. 1991. 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