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Phenotypes and the onset of competition in spring barley stands of one genotype: daylength and density effects on tillering
European Journal of Agronomy 12 (2000) 211 – 223 www.elsevier.com/locate/euragr
Phenotypes and the onset of competition in spring barley stands of one genotype: daylength and density effects on tillering M. Lafarge * INRA, Station d’Agronomie, 234 A6enue du Bre´zet, 63039 Clermont-Ferrand, France Received 21 June 1999; received in revised form 21 November 1999; accepted 26 January 2000
Abstract Understanding the genotype–environment interactions requires a distinction between two effects of the environment on plants of a given genotype: the achievement of growth throughout their whole life and the prior determination of their growth potentials. Spring barley seeds from the same seed lot were sown at the end of the winter at three altitudes: 320 m a.s.l. (end of February), 880 m (beginning of April) and 1120 m (beginning of May), and at the end of May at the lowest site, in sparse and dense stands with and without nitrogen fertilization. This experimental design in natural conditions gave differences in initial daylengths (12, 14 and more than 15 h) that must modify the growth potentials, and different levels of competition, acting on growth achievement. The tillering patterns were measured on individual plants. The tillers in the axils of the first and the second leaf were lacking on many plants growing in the long day treatments in the sparse stands, and this increased up to between 70 and 90% in the dense stands. This seems to be due to far-red signals on seedlings emerging in the conditions which induce the floral development, before any competition can occur. Afterwards, the cessation of tillering as a result of the onset of competition, was delayed markedly during stem elongation in the stands established with long daylengths. Such phenotypes showed strongly reduced growth potentials. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Spring barley; Phenotypes; Genotype–environment interactions; Tillering; Daylength; Neighbourhood; Competition
1. Introduction The growth potential of the plants proceeds from their genotype and its realization depends on their environment, but with interactions (Riggs, * Tel.: +33-473-624421; fax: + 33-473-624457. E-mail address: [email protected] (M. Lafarge)
1986) that reveal differences between growth capacities of genetically identical plants. Restricted growth capacities of the seedlings delay the onset of competition and thus a good use of resources at the canopy level (Boiffin et al., 1992). Low-potential or high-potential phenotypes may come from the same genotype, according to the seed quality (Ellis, 1992) or the environmental conditions occurring around seedling emergence (Cor-
1161-0301/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S 1 1 6 1 - 0 3 0 1 ( 0 0 ) 0 0 0 4 7 - 2
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nish and Lymbery, 1987; Durr et al., 1992). Some other early-set characters may be limiting too. For instance in spring barley, the earlier reproductive development in long daylength reduces the number of leaves (Kirby and Appleyard, 1980). Also, wheat plants that begin tillering at the node of the second true leaf bear shoots with lower growth capacity than plants with the first-leaf tiller (Masle-Meynard and Se´billotte, 1981a). At the same age, plants with delayed tillering start will bear fewer tillers and, thus, they will be less competitive in the stand. Distinguishing between the plant capacities induced during the early phase and later environmental growth restrictions will improve analyses of crop growth and genotype – environment interactions. The tiller number per plant is a result of competition for nitrogen or light (Masle, 1985). In fact, far-red signals from canopy closure (Casal et al., 1986) or from neighbouring plants (Casal et al., 1990) stop the tillering before any actual reduction in individual growth becomes evident. However, additional tillers produced by an artificial red-light enrichment under the canopy will not persist (Casal et al., 1986): far-red signals adapt the plant morphogenesis to an imminent shortage of carbon in naturally grown stands. The onset of competition can be back-dated to the time the tillering stopped (Kirby et al., 1985a). Twenty years ago, cereal growing was more common in the highland farms of the French Massif Central than it is at present (Lafarge, 1983). In that time, spring barley crops in two representative highland climates were compared to a lowland situation. The experimental locations build a gradient of initial daylengths that can hasten the development and reduce the growth capacities of the plants. This experiment was partly published (Lafarge, 1991, 1992), but the individual tillering measurements were not exploited. We try to distinguish between initial tillering characteristics (defining phenotypes) and characteristics indicating the cessation of tillering (and thus the onset of competition) in the tillering patterns recorded on the plants. We also try to link the cessation of tillering at the stand level to the distribution of phenotypes, and to link these early phenotypes to the experimental conditions.
2. Material and methods
2.1. Sites and experimental design The experimental design consisted of three sites around Clermont-Ferrand, in the French Massif Central. One is at 320 m a.s.l., ‘Malintrat’, on the commercial cereal-cropping plain, on an isohumic clay soil with a pH 8.2; it is the control lowland site. The next is at 880 m a.s.l., ‘St Gene`s’; this site has a brown-acid soil (pH 5.8) with a good availability of P and K. The last site is at 1120 m a.s.l., ‘Landeyrat’, in a summer-pasture area where combine-harvesting is risky; the andic soil (pH 5.4) have some exchangeable aluminium (0.7 meq%) and low phosphorus availability, but the experimental field was cultivated and well supplied with PK during the previous years. The two-rowed variety ‘Berenice’ was the spring barley genotype used in this experiment. All sowings were made from the same seed lot of the quality required for seed production. We drilled at the end of the winter 1978 at each location: on Febraury 24th at Malintrat (situation ME); on April 3rd at St Gene`s (situation SGE) and on May 3rd at Landeyrat (situation LE). At Malintrat, a later sowing was also carried out to provide a simultaneous stem elongation with the last sowing in the highlands (situation ML). This sowing was made on May 30th, with chemical protection against Frit fly (Oscinella frit L.). These four ‘situation treatments’ exposed the genotype to environmental variation which acts on plant potential and competition: the initial daylength influences the growth capacity and the risk of drought and the temperature influence the resource availability (Table 1). At each treatment site, conditions which influence competition were established with different sowing densities and nitrogen fertilizations. A sowing density of 150 grains m − 2 represented sparse stands. Dense stands were created from sowing densities which were increased at each progressive sowing date, in order to equalize the competition, considering the expected reductions in the plant growth capacities. These densities were 300 grains m − 2 at ME, 400 at SGE and 650 at LE and ML. Nitrogen fertilization was applied
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at a rate that would yield 7 t ha − 1 of grain, considering the resources available at each site. These resources were set by the nitrate content of the soil at the end of the winter (Re´my and He´bert, 1977): 110 kg N ha − 1 at Malintrat and St Gene`s, and 50 at Landeyrat. Thus, the rate of fertilizer application was 100 kg N ha − 1 for ME, SGE and ML, and 160 kg N ha − 1 for LE. Half this fertilizer was applied at plant emergence and the other half after the beginning of stem elongation. As alternative treatment at all sites, no fertilization was applied. The following four conditions of competition were applied everywhere: SO: sparse stand without nitrogen fertilizer; SN: nitrogen-fertilized sparse stand; DO: dense stand without nitrogen fertilizer; DN: nitrogen-fertilized dense stand.
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There were six replicates of each condition in each situation. The rows in each plot were spaced 25 cm apart in order to facilitate hoeing if chemical weed control was not effective. It was thought at the time of the experiment that spacing along the rows did not effect plant development.
2.2. Phenology and obser6ations The developmental stages of the apices were not systematically recorded. The phenological scale was very simple: the beginning of the stem elongation (‘ear-at-1 cm’ — Kirby et al., 1985b), the ear emergence (‘heading’) and the beginning of the grain ripening (‘pasty-ripe stage’). Samples of plant material were taken and measurements were done at each of these three stages. After the beginning of stem elongation, the frequency of
Table 1 The situation treatments (altitudes and sowing dates) as modalities of two factors: the initial daylength and the availability of soil resourcesa Initial daylength (12 h)
Initial daylength (14 h)
Initial daylength (\15 h)
Usual growth potential
Reduced growth potential
Low growth potential
Low risk of drought during stand formation: Soil resources always available
ME End-of-winter sowing at 320m
X
LE End-of-winter sowing at 1120 m
Some dry periods during stand formation: Occasional shortages of soil resources
X
SGE End-of-winter sowing at 880 m
X
High initial temperatures and high risk of drought during stand formation: Low source/sink ratio and availability of resources depending on rains
X
X
ML Late sowing at 320 m
a According to the effect of the daylength (Kirby and Appleyard, 1980), the growth potential is ‘usual’ when the plants emerge in the same daylength as in the areas of commercial cropping of spring barley, and ‘reduced’ when they emerge in longer days. The ‘low’ growth potential just refers to a greater reduction in even longer days. ME, SGE, LE and ML are the acronyms used in the next table and figures to refer to the situation treatments: end-of-winter sowings at Malintrat (320 m) = ME, at Saint Gene`s (880 m)=SGE, and at Landeyrat (1120 m)= LE. ML refers to the late sowing (May 30th) at Malintrat. ‘X’ means the lack of the modality. The risks of drought were estimated according to the usual climates during the pre-anthesis phase of spring barley crops at each location. At Malintrat and St Gene`s the rainfall is generally in excess in May. Afterwards, the drought is progressively rising. Spring barley crops sown at the end of the winter are usually at heading at the beginning of June (that is before any drought) at Malintrat, but at the end of June at St Gene`s, inducing risks of drought during stem elongation. Spring barley sown at the end of May at Malintrat will continuously grow under drought. At Landeyrat, the rainfall is usually nearly equal to the evapotranspiration throughout the spring and the summer.
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young tillers was surveyed roughly in the stands. When this frequency seemed to be low, the tillering was supposed to be slowing down and a sampling was done to describe the tillering pattern. At each sampling stage in each treatment site, 0.35 m×0.75 m=0.26 m2 of the stand was sampled from each plot. At the ‘ear-at-1 cm’ stage, plants were counted and all above-ground parts were dried and weighed. Around the apparent end of tillering, all the plants were counted and for 25 plants from each sample, the ‘tillering architecture’ was described as below (see Section 2.3). Next, at the ‘heading’ stage, all the ears were counted and all the above-ground parts were dried and weighed. Finally, at the ‘pasty-ripe’ stage, plants and ears were counted and enough plants to get 60 ear-bearing shoots were sub-sampled from each plot sample. In the sub-sample all the dead, ear-bearing and live non-ear-bearing shoots were counted on each plant.
2.3. Architecture and dynamics of the tillering On each plant of each ‘tillering architecture’ sub-sample, all emerged tillers were identified by the node which bore it (Kirby et al., 1985a): TC for the tiller on the coleoptile node, T1 for the tiller in the axil of the first leaf, and continuing with this rule. On each shoot axis (i.e. main stem or tillers), leaves were counted and the apex was noted as growing or dead. Afterwards, plants were classified according to the lowest node bearing a tiller, using the following codes: TC + for plants with a coleoptile tiller, T1 +, T2 + , T3 + for plants with their first tiller in the axil of the leaf 1, 2, 3 and WT for plants without tiller. T1 + is usually the most common type, but barley plants often bear TC (Cannell, 1969; Kirby et al., 1985a). Observed plant architectures were compared with the tillering model by Masle-Meynard and Se´billotte (1981b) validated for barley by Kirby et al. (1985a) and described on the Fig. 1 for each tillering type. Tillering types have the same timing; they differ by the node bearing the first primary tiller and, therefore, by the number of secondary and tertiary tillers that the plant can
bear at a given age. A specified tiller emerges at a given age of its mother axis: during unfolding of the ‘n’th leaf, the tiller in the axil of the ‘n− 3’th leaf emerges. For example, T2 appears (with one leaf) when the main stem bears five leaves; T11 (the secondary tiller in the axil of the first true leaf of T1) appears when T1 bears four leaves, and so on (the node of the coleoptile on the main stem and the node of the prophyll on the tillers are numbered 0). All shoots of a plant have almost the same phyllochron: all tillers in the same row on Fig. 1 emerge almost together: for example, in a T1+ type, the five tillers in the last row emerge during unfolding of the eighth leaf on the main stem. After the beginning of tillering, all successive tillers must emerge until tillering stops. Tillering cessation occurs at almost the same time on all shoot axes of the same plant. If some tillers at a given level in the hierarchy (Fig. 1) are lacking on a plant, then no tiller of the next row can be found. The tillering is stopped at the row where all tillers are lacking, that is at the corresponding phyllochron on the main stem (Kirby et al., 1985a). For example, a T1+ plant with seven leaves on its main stem at the sampling date but without T4, T11 nor T2p stopped its tillering at the current phyllochron. If the tillering architecture of a plant agrees with the model (i.e. the numbers of leaves correspond to a point in Fig. 1 and there was no break in the succession of tillers), it is possible to calculate the date tillering stopped for individual plants. Normally, after this cessation the rapid increase in competition between elongating shoots prevent resumption of any tillering in cereal plants (Masle, 1985), unlike the pasture grasses. Nevertheless, such a resumption is sometimes observable on barley when there is a sharp increase in resources (Aspinall, 1961). In that case, the tillering leaves the model. Leaves were counted with integer numbers; thus, a small difference in leaf unfolding rate between tillers can make the observed plants different from the model. Fortran-programmes were written to compare the observed architecture of each sampled plant to the model, with a tolerance of one leaf, to back date their cessation of tillering and to simulate additional tillering on plants, which continue to tiller at the sampling date.
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Fig. 1. Tillering models according to the node bearing the first tiller (adapted from Masle-Meynard and Se´billotte, 1981b; Kirby et al., 1985a). The tillering can continue over eight leaves on the main stem with the same rule. MS, main stem; TC, tiller at the coleoptile node; T1…T5, tillers in the axil of the first to the fifth true leaf of the main stem. TCp…T3p, secondary tillers in the axil of the prophyll of the specified primary tillers; (TC…T2)n, secondary tillers in the axil of the nth true leaf of the specified primary tillers. (TCp, TC1, T1p)p…1, tertiary tillers in the axil of the prophyll or in the axil of the first true leaf of the specified secondary tillers.
2.4. Growing conditions Soil temperatures during germination were close to 6°C for the three end-of-winter sowings
but much higher at ML (18°C). Crops emerged on March 12th at ME, on April 23rd at SGE and on May 21st at LE. ML plants emerged in two groups because they were sown in a dry seed bed.
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In all plots one third emerged on June 4th and the other two thirds on June 12th after rain. During the first days after plant emergence, the daylength was 12 h at ME, 14 h at SGE, 15 h 15 min at LE and 15 h 30 min at ML. Fig. 2 summarizes the climatic conditions from emergence to the first sampling date and between the successive sampling dates in each situation treatment. The parameters shown were the air temperature, the daily mean balance between rainfall and maximal evapotranspiration and the photothermal quotient. This quotient is the global radiation per degree-day; it is an indicator for source/sink ratio that can interact with daylength (Rawson, 1993). It was used by Fischer (1985) for comparisons between crops grown under very different climates. Light interceptions by the stands were not measured. All time lengths are expressed in thermal time with 0°C as base temperature (Gallagher et al., 1983).
3. Results
3.1. Crop phases and pre-anthesis stand biomasses Fig. 3 shows the crop phases for each situation
treatment and highlights the four sampling dates. Apart from ME, differences appeared between stand densities right from the beginning of shooting. The sampling dates represent a compromise for the actual beginnings of stem elongation. The ‘ear-at-1 cm’ stage was earlier at SGE and LE than at ME, especially in dense stands. The range of main-stem headings at ML is caused by the two emergence dates at that site while at LE the differences were among individual plants. The interval between the ‘ear-at-1 cm’ and the ‘tillering architecture’ samplings was a quarter of the thermal time between the ‘ear-at-1 cm’ and the ‘heading’ samplings at ME, SGE and LE, and 30% at ML. The stand biomasses of samples for the ‘heading’ stages (Fig. 4) were greater in the dense stands, regardless of the fertilizer regime, in the three long daylength treatments, especially at LE. The predicted limited individual growth capacity prevented the stand growth being fitted to the resources only. The dry mass of the ‘ear-at-1 cm’ samples in sparse stands (Fig. 4) is mainly in relation to the elapsed thermal time since emergence (see Fig. 3).
3.2. Tillering patterns and tillering types More than 96% of the plants at ME, SGE and
Fig. 2. Climatic conditions experienced by the crops in each cultural situation: mean air temperature (°C — stars), mean daily balance between rainfall and maximal evapotranspiration (mm — solid floating bargraphs) and photothermal quotient (global radiation in MJ m − 2 per degree-day — dotted bargraphs) in four consecutive periods from emergence to the last sampling date. Situation treatments: ME, SGE and LE, end-of-winter sowings at 320 m a.s.l., 880 m and 1120 m, respectively. ML, late sowing at 320 m a.s.l. (see Section 2.1). Periods: e1, from emergence to ‘ear-at-1 cm’ sampling date; 1t, from ‘ear-at-1 cm’ to ‘tillering architecture’ sampling dates; th, from ‘tillering architecture’ to ‘heading’ sampling dates; hp, from ‘heading’ to ‘pasty-ripe’ sampling dates.
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Fig. 3. Crop phases in each cultural situation and stand density. S, sparse stands; D, dense stands; ME, SGE, LE and ML, situation treatments as in Fig. 2. Samplings: 1, ear-at-1 cm; t, tillering architecture; h, heading; p, pasty-ripe. The dates of the plant emergence and of the samplings are on the right side of the bargraphs.
LE — and 94% at ML — conformed with the tillering model (see Section 2.3 and Fig. 1). Some of the plants without tillers only bore five leaves at the sampling time. It is possible for these plants to bear a tiller in the axil of the third leaf (T3)
during the unfolding of their sixth leaf (see Fig. 1); therefore, T3+ and WT tillering types cannot be distinguished. All tillering types can be found in all situation treatments. In all cropping conditions at ME and
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in sparse stands at SGE and ML more than 80% of the plants sampled were T1+ plants, and the other ones were mainly from the TC+ type, except at ML (Fig. 5). Dense stands at LE and ML consisted mostly of plants of the T2+ and WT&T3+ tillering types, that is plants with a delayed tillering start. In sparse stands, despite
high variability between plots, LE had significantly more T2+ and WT&T3+ tillering types than ME and SGE (Fig. 5). Long initial day length and high stand densities delayed the start of tillering: almost no TC+ plants at LE, ML and in dense stands of SGE, and very few T1+ plants in dense stands of LE
Fig. 4. Means ( 9S.E.) of stand dry masses of the ‘ear-at-1 cm’ and ‘heading’ samples (bar graphs), and the range of stand dry-masses observed by Biscoe et al. (1975) at the closure of spring barley canopies (hatched strip). ME, SGE, LE and ML, situation treatments as in Fig. 2 or Fig. 3. SO, SN, sparse stands without or with nitrogen fertilization; DO, DN, dense stands without or with nitrogen fertilization.
Fig. 5. Percent of plants (9S.E.) of each tillering type in each cultural situation and cropping condition. Tillering types: plants with its first tiller at the coleoptile node (TC + ), or in the axil of the first (T1 + ), the second (T2 + ) or the third (T3 + ) leaf and plants without any tiller (WT). WT and T3+ tillering types are grouped together because they are not distinguishable on all plants (see Section 3.2). ME, SGE, LE and ML, situation treatments as in Figs. 2 and 3 or Fig. 4. SO, SN, DO and DN, cropping conditions as in Fig. 4.
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and ML. Nitrogen fertiliser favoured an earlier start to tillering at all sites: there are more TC + plants at ME, and there are more T1+ plants at LE and in the dense stands of SGE with nitrogen supply (Fig. 5). Nevertheless, differences between sparse stands at LE and ML are not explainable by daylength, density or nitrogen.
3.3. Tillering dynamics Some plants which were already tillering were able to continue tillering after the sampling dates in May-sown situations, especially at LE and unlike ME and SGE. Many WT plants are still able to bear T3 in dense stands at LE and ML (Table 2). The rate of the tillering cessation was different: two phyllochrons were enough to stop the tillering of 88–97% of the bearing-tiller plants in all conditions of ME and SGE, but in LE sparse stands only 45 – 65% of these plants stopped their tillering in two phyllochrons. In the LE sparse stands, some plants started to tiller after others had stopped in a same sample plot (data not shown). The differences in shoot numbers between the ‘pasty-ripe’ samples and the ‘tillering architecture’ samples (Table 2) showed that the dynamics of the stand differed between situation treatments. At ME, a general and quick cessation of tillering occurred inside the first quarter of the duration of stem elongation. No more tillers appeared afterwards and the usual disappearance of dead tillers was observed in dense stands. In SGE sparse stands, 130 additional shoots per square meter must come from a late resumption of tillering after a general cessation which was observed at the beginning of stem elongation. In dense stands, some plants were still tillering at the ‘tillering architecture’ sampling date, but they stopped immediately afterwards. At LE, further tillering must have also occurred to account for the observed final numbers of shoots, even in dense stands. Many of the plants were still able to tiller in accordance with the model after the ‘tillering architecture’ sampling date. Except in SN conditions, a short time of further tillering is enough to produce the additional number of shoots which was observed at
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the ‘pasty-ripe’ stage, if all plants capable did, actually tiller (Table 2). In SN conditions, a quarter of the plants had to double the shoot number of the stand; with at least three phyllochrons required to end tillering (Table 2), the last tillering cessation occurred towards the ‘heading’ stage at the earliest. In dense stands, almost all plants that were able to tiller in the future were young WT plants. It is unlikely that most of these plants were beginning to tiller at this time. Therefore, more tillering time than one phyllochron would be needed on the other plants. At ML, many plants were capable of tillering after the ‘tillering architecture’ sampling date, but in reality no more shoots emerged afterwards (Table 2). The last tillering cessation occurred at the ‘tillering architecture’ sampling date.
4. Discussion
4.1. Canopy closure The observed stand biomasses (Fig. 4) are compared to the biomass range at canopy closure found by Biscoe et al. (1975). All canopies at ME and dense stands at SGE and ML are likely to have been closed before the ‘heading’ sampling. At LE, dense stands may have also been barely closed at the ‘heading’ stage, while the sparse stands remained open at this stage. The significant disappearance of many dead tillers in dense stands at ME and in DN conditions at SGE (Table 2) is consistent with a canopy closure earlier in these stands than in the others.
4.2. The beginning of the tillering: the conditioning of the phenotypes A tiller is already growing before it emerges. According to Malvoisin (1984), Skinner and Nelson (1994) the tiller bud begins to grow at the end of the elongation of the sheath of its subtending leaf, that is at the emergence of the next leaf. Thus, the TC bud begins to grow at the emergence of the first leaf, the T1 bud at the emergence of the second leaf, and so on. Two phyllochrons of growth within the subtending
220 Table 2 Percentage of plants which are still able to tiller within the model after the ‘tillering architecture’ sampling, changes in shoot number between ‘tillering architecture’ and ‘pasty-ripe’ samples, and additional tillering events when significantly more shoots were counted on the ‘pasty-ripe’ samplesa Situation treatment and cropping condition
Number of plants per square meter
Percent of plants that are able to tiller within the modelb after the ‘tillering architecture’ sampling (%)
Number of shoot axes per square meter at
Already tillering plants
‘Tillering Architecture’ sampling
(Significant differences)
WT pl. bearing five leaves
‘Pasty-ripe’ sampling
ME–SO ME–SN ME–DO ME–DN
124 128 287 269
0 0 1 0
0 0 0 0
801 795 1082 1251
n.s. n.s. \ \
712 909 901 979
– – –
SGE–SO SGE–SN SGE–DO SGE–DN
118 120 369 402
0 0 0 0
0 0 5 1
360 464 746 974
B B n.s. \
486 596 691 705
Till. resumption Till. resumption – –
LE–SO LE–SN LE–DO LE–DN
129 128 582 637
13 10 3 4
24 16 45 48
333 363 694 944
B B B B
534 770 934 1210
ML–SO ML–SN ML–DO ML–DN
127 126 540 526
3 3 1 0
1 0 33 46
563 652 833 929
n.s. n.s. n.s. n.s.
545 559 811 896
One phyllochron Three phyllochrons One phyllochron One phyllochron – – – –
a All shoot axes were numbered: dead, live non-ear-bearing and ear-bearing axes. A shoot axis is a tiller or a main stem. A few main stems can be dead. Phyllochron: elapsed thermal time between the emergence of two successive leaves. Ability to tiller is estimated and additional tillering duration is simulated according to the model by Masle-Meynard and Se´billotte (1981b) — see Section 2.3 and Fig. 1 in Section 2). ME, SGE, LE and ML, situation treatments as in Table 1 or Fig. 2; SO, SN, sparse stands without or with nitrogen fertilization; DO, DN, dense stands without or with nitrogen fertilization (as in Fig. 5). b The plants which were able to tiller within the model after the sampling date are: (a) the tillering plants that had not stopped to tiller at the sampling date; (b) the plants without tiller which bore less than six unfolded leaves. c Simulation was carried out for each plant which was able to tiller within the model. For each further phyllochron of simulated tillering on all plants able to tiller, the new tillers were added to the previous shoot number of the stand in each plot, and this sum was compared to the ‘pasty-ripe’ strength by anova.
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Additional tillering required by the final number of shoots: minimum length of the continuation within the modelc or late resumption of tillering
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sheath are subsequently needed before the first leaf of the tiller emerges (Fig. 1). Kirby and Faris (1972) observed that the elongation of the prophyll in the subtending sheath always ended in the emergence of the tiller. Young barley seedlings in the field are unlikely to experience the effects of nutritional shortage. This is because seed reserves satisfy their nutritional needs until 120 – 200 degree-days after germination (Metivier and Dale, 1977; Kullmann and Greef, 1992). At this time, the unfolding of the second leaf occurs with the usual phyllochrons at spring time sowing (Kirby et al., 1982). Therefore, nitrogen cannot be so short that cell division in the buds of the first tillers was prevented. The nitrogen effect which was reported above (in the last paragraph of Section 3.2) is not necessarily related to competition. It could be a hormonal effect: Samuelson et al. (1992) showed barley seminal roots to produce cytokinins when nitrates rise in the growing medium, and cytokinins favour tiller bud growth (Johnston and Jeffcoat, 1977). Neighbourhood effects may be related to light quality effects (Ballare´ et al., 1987; Casal et al., 1990). In the literature on the effect of light quality on tillering (e.g. Kasperbauer and Karlen, 1986; Barnes and Bugbee, 1991; Skinner and Simmons, 1993; Davis and Simmons, 1994) investigations on the beginning of tillering on seedlings were not reported. However, Davis and Simmons (1994) recorded the presence of specified tillers on their sampled plants. These results on May-sown barley show that the far-red-enriched light from 2 cm-neighbouring plants on a row in a stand, is enough to delay the start of tillering up to T2 on some plants. In shorter days, Kirby and Faris show that very high plant densities prevented TC bud development in barley (Kirby and Faris, 1972) and advanced floral initiation (Kirby and Faris, 1970). The earlier far-red enrichment from neighbourhood rather than from canopy closure (which usually signals the onset of competition) can condition phenotypes by delaying the onset of tillering in an interaction with floral initiation. One possible reason for this effect, is the production of gibberellins which inhibit tiller growth (Johnston and Jeffcoat, 1977). A flow of gibberellins is produced at floral initiation and this is
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triggered by increased daylength (Pharis et al., 1987) or the addition of far-red light (Deitzer et al., 1979). In the dense stands of SGE, LE and ML, 1 cm or less separated the plants in a row because of the 25-cm-spaced rows of the experimental design. Long days and close neighbourhood strongly interacted to advance shooting (Fig. 3) and to lock the first tiller buds (Fig. 5) in dense stands. In sparse stands, the small number of WT&T3+ plants at ML compared to LE (Fig. 5), in spite of the same daylength and density, can be explained by the low photothermal quotient at ML (Fig. 2): the developmental effect of inductive daylengths is weakened by low irradiance at a given temperature in spring barley (Aspinall and Paleg, 1963; Faris et al., 1969). With similar photothermal quotients, high nitrogen supply and low plant density, a markedly increased daylength produced a higher level of phenotypes with delayed start of tillering (compare SN conditions at ME and LE).
4.3. End of tillering, competition and growth capacities The dynamics of the cessation of tillering reflected the ways of the onset of competition which occurred in the stands. At LE, some plants stopped tillering early at the beginning of stem elongation while others continued, or some even began to tiller (see 3.3). When the canopy was not closed during stem elongation (Fig. 4), the competition remained very weak for a long time, except locally, among direct neighbours. This is consistent with a situation of reduced growth potential: when the growth without competition is low, the restriction of growth by the same arrangement of neighbours is reduced (results by Lindquist et al., 1994). In the dense stands, the tillering continued late, as in the sparse stands (Table 2). The general onset of competition was not hastened by four times higher plant density, because this density had brought too high proportion of weak phenotypes (WT&T3+ ) (Fig. 5). At SGE, the general cessation of tillering at the beginning of stem elongation was likely due to
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competition for restricted soil resources, because of a sudden drought at that time (Fig. 2). Afterwards, in sparse stands the late closure of the canopy may have allowed for a resumption of tillering — such as in pasture grasses — as a consequence of rains after the drought (Luebs and Laag, 1969). In dense stands, the earlier closure of the canopy prevented the resumption of tillering. In these stands, three times higher plant density caused more weak phenotypes (Fig. 5), but started an earlier onset of competition (Table 2). At ME, the early and definitive cessation of tillering reflected an early establishment of competition between all plants, including the sparse stands, as a result of the high growth potential of the individuals. At ML, the tillering phenotypes seem to be close to those of SGE in sparse stands and to those of LE in dense stands (Fig. 5). In spite of these likely low growth potentials, no significant further tillering was observed (Table 2). Competition must have been established by soil resources restricted by long-lasting drought (Fig. 2).
5. Conclusions In sparse stands, long days at plant emergence highly increased the level of tillering phenotypes with low potentials. That resulted in a delayed markedly onset of competition. The environmental factors usually acting on growth and competition (nitrogen and above all plant density) interacted with daylength on emerging seedlings and modified the phenotype and the growth potential of the plants. As shown through the dynamics of the cessation of tillering, increased plant density, which was expected to compensate for the reduced growth capacities of plants emerging in long days, further reduced these initial growth capacities. Before carrying out the growth, the environmental conditions have differentiated the growth potentials of spring barley plants with the same genotype. When the daylength and the proximity of nearest neighbours interacted, this growth potential was reduced strongly.
Acknowledgements I thank E. Albaret, V. Andre´, G. Bielicki, B. Carette, D. Ezard, J. Hanoteaux, M. Louyot, A. Mante and C. Pravin for their technical assistance, and two anonymous referees for comments on an earlier version of this paper. I am also indebted to Jill Carter for revising the English of the manuscript.
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Lafarge, M., 1992. Vitesse d’e´mission des feuilles des brins maıˆtres d’une orge de printemps cultive´e a` plusieurs altitudes: diffe´rences lie´es au type de tallage et aux milieux. Agronomie 12, 691 – 703. Lindquist, J.L., Rhode, D., Puettmann, K.J., Maxwell, B.D., 1994. The influence of plant population spatial arrangement on individual plant yield. Ecol. Appl. 4, 518 – 524. Luebs, R.E., Laag, A.E., 1969. Evapotranspiration and water stress of barley with increased nitrogen. Agron. J. 61, 921 – 924. Malvoisin, P., 1984. Organoge´ne`se et croissance du maıˆtre brin du ble´ tendre (Triticum aesti6um) du semis a` la floraison. 2. Controˆle des relations entre la croissance et la vascularisation de la tige et des feuilles. Essai de mode´lisation. Agronomie 4, 587 – 596. Masle, J., 1985. Competition among tillers in winter wheat: consequences for growth and development of the crop. In: Day, W., Atkin, R.K. (Eds.), Wheat Growth and Modelling. NATO ASI Serie A, vol. 86. Plenum Press, New York, pp. 33 – 54. Masle-Meynard, J.and, Se´billotte, M., 1981a. Etude de l’he´te´roge´ne´ite´ d’un peuplement de ble´ d’hiver. 1. Notion de structure du peuplement. Agronomie 1, 207 – 216. Masle-Meynard, J., Se´billotte, M., 1981b. Etude de l’he´te´roge´ne´ite´ d’un peuplement de ble´ d’hiver. 2. Origine des diffe´rentes cate´gories d’individus du peuplement; e´le´ments de description de sa structure. Agronomie 1, 217 – 224. Metivier, J.R., Dale, J.E., 1977. The utilization of endosperm reserves during early growth of barley cultivars and the effect of time of application of nitrogen. Ann. Bot. 41, 715 – 728. Pharis, R.P., Evans, L.T., King, R.W., Mander, L.N., 1987. Gibberellins, endogenous and applied, in relation to flower induction in the long-day plant Lolium tementulum. Plant Physiol. 84, 1132 – 1138. Rawson, H.M., 1993. Radiation effects on rate of development in wheat grown under different photoperiods and high and low temperatures. Aust. J. Plant Physiol. 20, 719 – 727. Re´my, J.C., He´bert, J., 1977. Le devenir des engrais azote´s dans le sol. C. R. Acad. Agric. Fr. 63, 700 – 714. Riggs, T.J., 1986. Collaborative spring barley trials in Europe 1980 – 82. Analysis of grain yield. Z. Pflanzenzu¨chtg 96, 289 – 303. Samuelson, M.E., Eliasson, L., Larsson, C.M., 1992. Nitrateregulated growth and cytokinin responses in seminal roots of barley. Plant Physiol. 98, 309 – 315. Skinner, R.H., Nelson, C.J., 1994. Epidermal cell division and the coordination of leaf and tiller development. Ann. Bot. 74, 9 – 15. Skinner, R.H., Simmons, S.R., 1993. Modulation of leaf elongation, tiller appearance and tiller senescence in spring barley by far-red light. Plant Cell Environ. 16, 555 – 562.
Phenotypes and the onset of competition in spring barley stands of one genotype: daylength and density effects on tillering M. Lafarge * INRA, Station d’Agronomie, 234 A6enue du Bre´zet, 63039 Clermont-Ferrand, France Received 21 June 1999; received in revised form 21 November 1999; accepted 26 January 2000
Abstract Understanding the genotype–environment interactions requires a distinction between two effects of the environment on plants of a given genotype: the achievement of growth throughout their whole life and the prior determination of their growth potentials. Spring barley seeds from the same seed lot were sown at the end of the winter at three altitudes: 320 m a.s.l. (end of February), 880 m (beginning of April) and 1120 m (beginning of May), and at the end of May at the lowest site, in sparse and dense stands with and without nitrogen fertilization. This experimental design in natural conditions gave differences in initial daylengths (12, 14 and more than 15 h) that must modify the growth potentials, and different levels of competition, acting on growth achievement. The tillering patterns were measured on individual plants. The tillers in the axils of the first and the second leaf were lacking on many plants growing in the long day treatments in the sparse stands, and this increased up to between 70 and 90% in the dense stands. This seems to be due to far-red signals on seedlings emerging in the conditions which induce the floral development, before any competition can occur. Afterwards, the cessation of tillering as a result of the onset of competition, was delayed markedly during stem elongation in the stands established with long daylengths. Such phenotypes showed strongly reduced growth potentials. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Spring barley; Phenotypes; Genotype–environment interactions; Tillering; Daylength; Neighbourhood; Competition
1. Introduction The growth potential of the plants proceeds from their genotype and its realization depends on their environment, but with interactions (Riggs, * Tel.: +33-473-624421; fax: + 33-473-624457. E-mail address: [email protected] (M. Lafarge)
1986) that reveal differences between growth capacities of genetically identical plants. Restricted growth capacities of the seedlings delay the onset of competition and thus a good use of resources at the canopy level (Boiffin et al., 1992). Low-potential or high-potential phenotypes may come from the same genotype, according to the seed quality (Ellis, 1992) or the environmental conditions occurring around seedling emergence (Cor-
1161-0301/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S 1 1 6 1 - 0 3 0 1 ( 0 0 ) 0 0 0 4 7 - 2
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nish and Lymbery, 1987; Durr et al., 1992). Some other early-set characters may be limiting too. For instance in spring barley, the earlier reproductive development in long daylength reduces the number of leaves (Kirby and Appleyard, 1980). Also, wheat plants that begin tillering at the node of the second true leaf bear shoots with lower growth capacity than plants with the first-leaf tiller (Masle-Meynard and Se´billotte, 1981a). At the same age, plants with delayed tillering start will bear fewer tillers and, thus, they will be less competitive in the stand. Distinguishing between the plant capacities induced during the early phase and later environmental growth restrictions will improve analyses of crop growth and genotype – environment interactions. The tiller number per plant is a result of competition for nitrogen or light (Masle, 1985). In fact, far-red signals from canopy closure (Casal et al., 1986) or from neighbouring plants (Casal et al., 1990) stop the tillering before any actual reduction in individual growth becomes evident. However, additional tillers produced by an artificial red-light enrichment under the canopy will not persist (Casal et al., 1986): far-red signals adapt the plant morphogenesis to an imminent shortage of carbon in naturally grown stands. The onset of competition can be back-dated to the time the tillering stopped (Kirby et al., 1985a). Twenty years ago, cereal growing was more common in the highland farms of the French Massif Central than it is at present (Lafarge, 1983). In that time, spring barley crops in two representative highland climates were compared to a lowland situation. The experimental locations build a gradient of initial daylengths that can hasten the development and reduce the growth capacities of the plants. This experiment was partly published (Lafarge, 1991, 1992), but the individual tillering measurements were not exploited. We try to distinguish between initial tillering characteristics (defining phenotypes) and characteristics indicating the cessation of tillering (and thus the onset of competition) in the tillering patterns recorded on the plants. We also try to link the cessation of tillering at the stand level to the distribution of phenotypes, and to link these early phenotypes to the experimental conditions.
2. Material and methods
2.1. Sites and experimental design The experimental design consisted of three sites around Clermont-Ferrand, in the French Massif Central. One is at 320 m a.s.l., ‘Malintrat’, on the commercial cereal-cropping plain, on an isohumic clay soil with a pH 8.2; it is the control lowland site. The next is at 880 m a.s.l., ‘St Gene`s’; this site has a brown-acid soil (pH 5.8) with a good availability of P and K. The last site is at 1120 m a.s.l., ‘Landeyrat’, in a summer-pasture area where combine-harvesting is risky; the andic soil (pH 5.4) have some exchangeable aluminium (0.7 meq%) and low phosphorus availability, but the experimental field was cultivated and well supplied with PK during the previous years. The two-rowed variety ‘Berenice’ was the spring barley genotype used in this experiment. All sowings were made from the same seed lot of the quality required for seed production. We drilled at the end of the winter 1978 at each location: on Febraury 24th at Malintrat (situation ME); on April 3rd at St Gene`s (situation SGE) and on May 3rd at Landeyrat (situation LE). At Malintrat, a later sowing was also carried out to provide a simultaneous stem elongation with the last sowing in the highlands (situation ML). This sowing was made on May 30th, with chemical protection against Frit fly (Oscinella frit L.). These four ‘situation treatments’ exposed the genotype to environmental variation which acts on plant potential and competition: the initial daylength influences the growth capacity and the risk of drought and the temperature influence the resource availability (Table 1). At each treatment site, conditions which influence competition were established with different sowing densities and nitrogen fertilizations. A sowing density of 150 grains m − 2 represented sparse stands. Dense stands were created from sowing densities which were increased at each progressive sowing date, in order to equalize the competition, considering the expected reductions in the plant growth capacities. These densities were 300 grains m − 2 at ME, 400 at SGE and 650 at LE and ML. Nitrogen fertilization was applied
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at a rate that would yield 7 t ha − 1 of grain, considering the resources available at each site. These resources were set by the nitrate content of the soil at the end of the winter (Re´my and He´bert, 1977): 110 kg N ha − 1 at Malintrat and St Gene`s, and 50 at Landeyrat. Thus, the rate of fertilizer application was 100 kg N ha − 1 for ME, SGE and ML, and 160 kg N ha − 1 for LE. Half this fertilizer was applied at plant emergence and the other half after the beginning of stem elongation. As alternative treatment at all sites, no fertilization was applied. The following four conditions of competition were applied everywhere: SO: sparse stand without nitrogen fertilizer; SN: nitrogen-fertilized sparse stand; DO: dense stand without nitrogen fertilizer; DN: nitrogen-fertilized dense stand.
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There were six replicates of each condition in each situation. The rows in each plot were spaced 25 cm apart in order to facilitate hoeing if chemical weed control was not effective. It was thought at the time of the experiment that spacing along the rows did not effect plant development.
2.2. Phenology and obser6ations The developmental stages of the apices were not systematically recorded. The phenological scale was very simple: the beginning of the stem elongation (‘ear-at-1 cm’ — Kirby et al., 1985b), the ear emergence (‘heading’) and the beginning of the grain ripening (‘pasty-ripe stage’). Samples of plant material were taken and measurements were done at each of these three stages. After the beginning of stem elongation, the frequency of
Table 1 The situation treatments (altitudes and sowing dates) as modalities of two factors: the initial daylength and the availability of soil resourcesa Initial daylength (12 h)
Initial daylength (14 h)
Initial daylength (\15 h)
Usual growth potential
Reduced growth potential
Low growth potential
Low risk of drought during stand formation: Soil resources always available
ME End-of-winter sowing at 320m
X
LE End-of-winter sowing at 1120 m
Some dry periods during stand formation: Occasional shortages of soil resources
X
SGE End-of-winter sowing at 880 m
X
High initial temperatures and high risk of drought during stand formation: Low source/sink ratio and availability of resources depending on rains
X
X
ML Late sowing at 320 m
a According to the effect of the daylength (Kirby and Appleyard, 1980), the growth potential is ‘usual’ when the plants emerge in the same daylength as in the areas of commercial cropping of spring barley, and ‘reduced’ when they emerge in longer days. The ‘low’ growth potential just refers to a greater reduction in even longer days. ME, SGE, LE and ML are the acronyms used in the next table and figures to refer to the situation treatments: end-of-winter sowings at Malintrat (320 m) = ME, at Saint Gene`s (880 m)=SGE, and at Landeyrat (1120 m)= LE. ML refers to the late sowing (May 30th) at Malintrat. ‘X’ means the lack of the modality. The risks of drought were estimated according to the usual climates during the pre-anthesis phase of spring barley crops at each location. At Malintrat and St Gene`s the rainfall is generally in excess in May. Afterwards, the drought is progressively rising. Spring barley crops sown at the end of the winter are usually at heading at the beginning of June (that is before any drought) at Malintrat, but at the end of June at St Gene`s, inducing risks of drought during stem elongation. Spring barley sown at the end of May at Malintrat will continuously grow under drought. At Landeyrat, the rainfall is usually nearly equal to the evapotranspiration throughout the spring and the summer.
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young tillers was surveyed roughly in the stands. When this frequency seemed to be low, the tillering was supposed to be slowing down and a sampling was done to describe the tillering pattern. At each sampling stage in each treatment site, 0.35 m×0.75 m=0.26 m2 of the stand was sampled from each plot. At the ‘ear-at-1 cm’ stage, plants were counted and all above-ground parts were dried and weighed. Around the apparent end of tillering, all the plants were counted and for 25 plants from each sample, the ‘tillering architecture’ was described as below (see Section 2.3). Next, at the ‘heading’ stage, all the ears were counted and all the above-ground parts were dried and weighed. Finally, at the ‘pasty-ripe’ stage, plants and ears were counted and enough plants to get 60 ear-bearing shoots were sub-sampled from each plot sample. In the sub-sample all the dead, ear-bearing and live non-ear-bearing shoots were counted on each plant.
2.3. Architecture and dynamics of the tillering On each plant of each ‘tillering architecture’ sub-sample, all emerged tillers were identified by the node which bore it (Kirby et al., 1985a): TC for the tiller on the coleoptile node, T1 for the tiller in the axil of the first leaf, and continuing with this rule. On each shoot axis (i.e. main stem or tillers), leaves were counted and the apex was noted as growing or dead. Afterwards, plants were classified according to the lowest node bearing a tiller, using the following codes: TC + for plants with a coleoptile tiller, T1 +, T2 + , T3 + for plants with their first tiller in the axil of the leaf 1, 2, 3 and WT for plants without tiller. T1 + is usually the most common type, but barley plants often bear TC (Cannell, 1969; Kirby et al., 1985a). Observed plant architectures were compared with the tillering model by Masle-Meynard and Se´billotte (1981b) validated for barley by Kirby et al. (1985a) and described on the Fig. 1 for each tillering type. Tillering types have the same timing; they differ by the node bearing the first primary tiller and, therefore, by the number of secondary and tertiary tillers that the plant can
bear at a given age. A specified tiller emerges at a given age of its mother axis: during unfolding of the ‘n’th leaf, the tiller in the axil of the ‘n− 3’th leaf emerges. For example, T2 appears (with one leaf) when the main stem bears five leaves; T11 (the secondary tiller in the axil of the first true leaf of T1) appears when T1 bears four leaves, and so on (the node of the coleoptile on the main stem and the node of the prophyll on the tillers are numbered 0). All shoots of a plant have almost the same phyllochron: all tillers in the same row on Fig. 1 emerge almost together: for example, in a T1+ type, the five tillers in the last row emerge during unfolding of the eighth leaf on the main stem. After the beginning of tillering, all successive tillers must emerge until tillering stops. Tillering cessation occurs at almost the same time on all shoot axes of the same plant. If some tillers at a given level in the hierarchy (Fig. 1) are lacking on a plant, then no tiller of the next row can be found. The tillering is stopped at the row where all tillers are lacking, that is at the corresponding phyllochron on the main stem (Kirby et al., 1985a). For example, a T1+ plant with seven leaves on its main stem at the sampling date but without T4, T11 nor T2p stopped its tillering at the current phyllochron. If the tillering architecture of a plant agrees with the model (i.e. the numbers of leaves correspond to a point in Fig. 1 and there was no break in the succession of tillers), it is possible to calculate the date tillering stopped for individual plants. Normally, after this cessation the rapid increase in competition between elongating shoots prevent resumption of any tillering in cereal plants (Masle, 1985), unlike the pasture grasses. Nevertheless, such a resumption is sometimes observable on barley when there is a sharp increase in resources (Aspinall, 1961). In that case, the tillering leaves the model. Leaves were counted with integer numbers; thus, a small difference in leaf unfolding rate between tillers can make the observed plants different from the model. Fortran-programmes were written to compare the observed architecture of each sampled plant to the model, with a tolerance of one leaf, to back date their cessation of tillering and to simulate additional tillering on plants, which continue to tiller at the sampling date.
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Fig. 1. Tillering models according to the node bearing the first tiller (adapted from Masle-Meynard and Se´billotte, 1981b; Kirby et al., 1985a). The tillering can continue over eight leaves on the main stem with the same rule. MS, main stem; TC, tiller at the coleoptile node; T1…T5, tillers in the axil of the first to the fifth true leaf of the main stem. TCp…T3p, secondary tillers in the axil of the prophyll of the specified primary tillers; (TC…T2)n, secondary tillers in the axil of the nth true leaf of the specified primary tillers. (TCp, TC1, T1p)p…1, tertiary tillers in the axil of the prophyll or in the axil of the first true leaf of the specified secondary tillers.
2.4. Growing conditions Soil temperatures during germination were close to 6°C for the three end-of-winter sowings
but much higher at ML (18°C). Crops emerged on March 12th at ME, on April 23rd at SGE and on May 21st at LE. ML plants emerged in two groups because they were sown in a dry seed bed.
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In all plots one third emerged on June 4th and the other two thirds on June 12th after rain. During the first days after plant emergence, the daylength was 12 h at ME, 14 h at SGE, 15 h 15 min at LE and 15 h 30 min at ML. Fig. 2 summarizes the climatic conditions from emergence to the first sampling date and between the successive sampling dates in each situation treatment. The parameters shown were the air temperature, the daily mean balance between rainfall and maximal evapotranspiration and the photothermal quotient. This quotient is the global radiation per degree-day; it is an indicator for source/sink ratio that can interact with daylength (Rawson, 1993). It was used by Fischer (1985) for comparisons between crops grown under very different climates. Light interceptions by the stands were not measured. All time lengths are expressed in thermal time with 0°C as base temperature (Gallagher et al., 1983).
3. Results
3.1. Crop phases and pre-anthesis stand biomasses Fig. 3 shows the crop phases for each situation
treatment and highlights the four sampling dates. Apart from ME, differences appeared between stand densities right from the beginning of shooting. The sampling dates represent a compromise for the actual beginnings of stem elongation. The ‘ear-at-1 cm’ stage was earlier at SGE and LE than at ME, especially in dense stands. The range of main-stem headings at ML is caused by the two emergence dates at that site while at LE the differences were among individual plants. The interval between the ‘ear-at-1 cm’ and the ‘tillering architecture’ samplings was a quarter of the thermal time between the ‘ear-at-1 cm’ and the ‘heading’ samplings at ME, SGE and LE, and 30% at ML. The stand biomasses of samples for the ‘heading’ stages (Fig. 4) were greater in the dense stands, regardless of the fertilizer regime, in the three long daylength treatments, especially at LE. The predicted limited individual growth capacity prevented the stand growth being fitted to the resources only. The dry mass of the ‘ear-at-1 cm’ samples in sparse stands (Fig. 4) is mainly in relation to the elapsed thermal time since emergence (see Fig. 3).
3.2. Tillering patterns and tillering types More than 96% of the plants at ME, SGE and
Fig. 2. Climatic conditions experienced by the crops in each cultural situation: mean air temperature (°C — stars), mean daily balance between rainfall and maximal evapotranspiration (mm — solid floating bargraphs) and photothermal quotient (global radiation in MJ m − 2 per degree-day — dotted bargraphs) in four consecutive periods from emergence to the last sampling date. Situation treatments: ME, SGE and LE, end-of-winter sowings at 320 m a.s.l., 880 m and 1120 m, respectively. ML, late sowing at 320 m a.s.l. (see Section 2.1). Periods: e1, from emergence to ‘ear-at-1 cm’ sampling date; 1t, from ‘ear-at-1 cm’ to ‘tillering architecture’ sampling dates; th, from ‘tillering architecture’ to ‘heading’ sampling dates; hp, from ‘heading’ to ‘pasty-ripe’ sampling dates.
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Fig. 3. Crop phases in each cultural situation and stand density. S, sparse stands; D, dense stands; ME, SGE, LE and ML, situation treatments as in Fig. 2. Samplings: 1, ear-at-1 cm; t, tillering architecture; h, heading; p, pasty-ripe. The dates of the plant emergence and of the samplings are on the right side of the bargraphs.
LE — and 94% at ML — conformed with the tillering model (see Section 2.3 and Fig. 1). Some of the plants without tillers only bore five leaves at the sampling time. It is possible for these plants to bear a tiller in the axil of the third leaf (T3)
during the unfolding of their sixth leaf (see Fig. 1); therefore, T3+ and WT tillering types cannot be distinguished. All tillering types can be found in all situation treatments. In all cropping conditions at ME and
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in sparse stands at SGE and ML more than 80% of the plants sampled were T1+ plants, and the other ones were mainly from the TC+ type, except at ML (Fig. 5). Dense stands at LE and ML consisted mostly of plants of the T2+ and WT&T3+ tillering types, that is plants with a delayed tillering start. In sparse stands, despite
high variability between plots, LE had significantly more T2+ and WT&T3+ tillering types than ME and SGE (Fig. 5). Long initial day length and high stand densities delayed the start of tillering: almost no TC+ plants at LE, ML and in dense stands of SGE, and very few T1+ plants in dense stands of LE
Fig. 4. Means ( 9S.E.) of stand dry masses of the ‘ear-at-1 cm’ and ‘heading’ samples (bar graphs), and the range of stand dry-masses observed by Biscoe et al. (1975) at the closure of spring barley canopies (hatched strip). ME, SGE, LE and ML, situation treatments as in Fig. 2 or Fig. 3. SO, SN, sparse stands without or with nitrogen fertilization; DO, DN, dense stands without or with nitrogen fertilization.
Fig. 5. Percent of plants (9S.E.) of each tillering type in each cultural situation and cropping condition. Tillering types: plants with its first tiller at the coleoptile node (TC + ), or in the axil of the first (T1 + ), the second (T2 + ) or the third (T3 + ) leaf and plants without any tiller (WT). WT and T3+ tillering types are grouped together because they are not distinguishable on all plants (see Section 3.2). ME, SGE, LE and ML, situation treatments as in Figs. 2 and 3 or Fig. 4. SO, SN, DO and DN, cropping conditions as in Fig. 4.
M. Lafarge / Europ. J. Agronomy 12 (2000) 211–223
and ML. Nitrogen fertiliser favoured an earlier start to tillering at all sites: there are more TC + plants at ME, and there are more T1+ plants at LE and in the dense stands of SGE with nitrogen supply (Fig. 5). Nevertheless, differences between sparse stands at LE and ML are not explainable by daylength, density or nitrogen.
3.3. Tillering dynamics Some plants which were already tillering were able to continue tillering after the sampling dates in May-sown situations, especially at LE and unlike ME and SGE. Many WT plants are still able to bear T3 in dense stands at LE and ML (Table 2). The rate of the tillering cessation was different: two phyllochrons were enough to stop the tillering of 88–97% of the bearing-tiller plants in all conditions of ME and SGE, but in LE sparse stands only 45 – 65% of these plants stopped their tillering in two phyllochrons. In the LE sparse stands, some plants started to tiller after others had stopped in a same sample plot (data not shown). The differences in shoot numbers between the ‘pasty-ripe’ samples and the ‘tillering architecture’ samples (Table 2) showed that the dynamics of the stand differed between situation treatments. At ME, a general and quick cessation of tillering occurred inside the first quarter of the duration of stem elongation. No more tillers appeared afterwards and the usual disappearance of dead tillers was observed in dense stands. In SGE sparse stands, 130 additional shoots per square meter must come from a late resumption of tillering after a general cessation which was observed at the beginning of stem elongation. In dense stands, some plants were still tillering at the ‘tillering architecture’ sampling date, but they stopped immediately afterwards. At LE, further tillering must have also occurred to account for the observed final numbers of shoots, even in dense stands. Many of the plants were still able to tiller in accordance with the model after the ‘tillering architecture’ sampling date. Except in SN conditions, a short time of further tillering is enough to produce the additional number of shoots which was observed at
219
the ‘pasty-ripe’ stage, if all plants capable did, actually tiller (Table 2). In SN conditions, a quarter of the plants had to double the shoot number of the stand; with at least three phyllochrons required to end tillering (Table 2), the last tillering cessation occurred towards the ‘heading’ stage at the earliest. In dense stands, almost all plants that were able to tiller in the future were young WT plants. It is unlikely that most of these plants were beginning to tiller at this time. Therefore, more tillering time than one phyllochron would be needed on the other plants. At ML, many plants were capable of tillering after the ‘tillering architecture’ sampling date, but in reality no more shoots emerged afterwards (Table 2). The last tillering cessation occurred at the ‘tillering architecture’ sampling date.
4. Discussion
4.1. Canopy closure The observed stand biomasses (Fig. 4) are compared to the biomass range at canopy closure found by Biscoe et al. (1975). All canopies at ME and dense stands at SGE and ML are likely to have been closed before the ‘heading’ sampling. At LE, dense stands may have also been barely closed at the ‘heading’ stage, while the sparse stands remained open at this stage. The significant disappearance of many dead tillers in dense stands at ME and in DN conditions at SGE (Table 2) is consistent with a canopy closure earlier in these stands than in the others.
4.2. The beginning of the tillering: the conditioning of the phenotypes A tiller is already growing before it emerges. According to Malvoisin (1984), Skinner and Nelson (1994) the tiller bud begins to grow at the end of the elongation of the sheath of its subtending leaf, that is at the emergence of the next leaf. Thus, the TC bud begins to grow at the emergence of the first leaf, the T1 bud at the emergence of the second leaf, and so on. Two phyllochrons of growth within the subtending
220 Table 2 Percentage of plants which are still able to tiller within the model after the ‘tillering architecture’ sampling, changes in shoot number between ‘tillering architecture’ and ‘pasty-ripe’ samples, and additional tillering events when significantly more shoots were counted on the ‘pasty-ripe’ samplesa Situation treatment and cropping condition
Number of plants per square meter
Percent of plants that are able to tiller within the modelb after the ‘tillering architecture’ sampling (%)
Number of shoot axes per square meter at
Already tillering plants
‘Tillering Architecture’ sampling
(Significant differences)
WT pl. bearing five leaves
‘Pasty-ripe’ sampling
ME–SO ME–SN ME–DO ME–DN
124 128 287 269
0 0 1 0
0 0 0 0
801 795 1082 1251
n.s. n.s. \ \
712 909 901 979
– – –
SGE–SO SGE–SN SGE–DO SGE–DN
118 120 369 402
0 0 0 0
0 0 5 1
360 464 746 974
B B n.s. \
486 596 691 705
Till. resumption Till. resumption – –
LE–SO LE–SN LE–DO LE–DN
129 128 582 637
13 10 3 4
24 16 45 48
333 363 694 944
B B B B
534 770 934 1210
ML–SO ML–SN ML–DO ML–DN
127 126 540 526
3 3 1 0
1 0 33 46
563 652 833 929
n.s. n.s. n.s. n.s.
545 559 811 896
One phyllochron Three phyllochrons One phyllochron One phyllochron – – – –
a All shoot axes were numbered: dead, live non-ear-bearing and ear-bearing axes. A shoot axis is a tiller or a main stem. A few main stems can be dead. Phyllochron: elapsed thermal time between the emergence of two successive leaves. Ability to tiller is estimated and additional tillering duration is simulated according to the model by Masle-Meynard and Se´billotte (1981b) — see Section 2.3 and Fig. 1 in Section 2). ME, SGE, LE and ML, situation treatments as in Table 1 or Fig. 2; SO, SN, sparse stands without or with nitrogen fertilization; DO, DN, dense stands without or with nitrogen fertilization (as in Fig. 5). b The plants which were able to tiller within the model after the sampling date are: (a) the tillering plants that had not stopped to tiller at the sampling date; (b) the plants without tiller which bore less than six unfolded leaves. c Simulation was carried out for each plant which was able to tiller within the model. For each further phyllochron of simulated tillering on all plants able to tiller, the new tillers were added to the previous shoot number of the stand in each plot, and this sum was compared to the ‘pasty-ripe’ strength by anova.
M. Lafarge / Europ. J. Agronomy 12 (2000) 211–223
Additional tillering required by the final number of shoots: minimum length of the continuation within the modelc or late resumption of tillering
M. Lafarge / Europ. J. Agronomy 12 (2000) 211–223
sheath are subsequently needed before the first leaf of the tiller emerges (Fig. 1). Kirby and Faris (1972) observed that the elongation of the prophyll in the subtending sheath always ended in the emergence of the tiller. Young barley seedlings in the field are unlikely to experience the effects of nutritional shortage. This is because seed reserves satisfy their nutritional needs until 120 – 200 degree-days after germination (Metivier and Dale, 1977; Kullmann and Greef, 1992). At this time, the unfolding of the second leaf occurs with the usual phyllochrons at spring time sowing (Kirby et al., 1982). Therefore, nitrogen cannot be so short that cell division in the buds of the first tillers was prevented. The nitrogen effect which was reported above (in the last paragraph of Section 3.2) is not necessarily related to competition. It could be a hormonal effect: Samuelson et al. (1992) showed barley seminal roots to produce cytokinins when nitrates rise in the growing medium, and cytokinins favour tiller bud growth (Johnston and Jeffcoat, 1977). Neighbourhood effects may be related to light quality effects (Ballare´ et al., 1987; Casal et al., 1990). In the literature on the effect of light quality on tillering (e.g. Kasperbauer and Karlen, 1986; Barnes and Bugbee, 1991; Skinner and Simmons, 1993; Davis and Simmons, 1994) investigations on the beginning of tillering on seedlings were not reported. However, Davis and Simmons (1994) recorded the presence of specified tillers on their sampled plants. These results on May-sown barley show that the far-red-enriched light from 2 cm-neighbouring plants on a row in a stand, is enough to delay the start of tillering up to T2 on some plants. In shorter days, Kirby and Faris show that very high plant densities prevented TC bud development in barley (Kirby and Faris, 1972) and advanced floral initiation (Kirby and Faris, 1970). The earlier far-red enrichment from neighbourhood rather than from canopy closure (which usually signals the onset of competition) can condition phenotypes by delaying the onset of tillering in an interaction with floral initiation. One possible reason for this effect, is the production of gibberellins which inhibit tiller growth (Johnston and Jeffcoat, 1977). A flow of gibberellins is produced at floral initiation and this is
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triggered by increased daylength (Pharis et al., 1987) or the addition of far-red light (Deitzer et al., 1979). In the dense stands of SGE, LE and ML, 1 cm or less separated the plants in a row because of the 25-cm-spaced rows of the experimental design. Long days and close neighbourhood strongly interacted to advance shooting (Fig. 3) and to lock the first tiller buds (Fig. 5) in dense stands. In sparse stands, the small number of WT&T3+ plants at ML compared to LE (Fig. 5), in spite of the same daylength and density, can be explained by the low photothermal quotient at ML (Fig. 2): the developmental effect of inductive daylengths is weakened by low irradiance at a given temperature in spring barley (Aspinall and Paleg, 1963; Faris et al., 1969). With similar photothermal quotients, high nitrogen supply and low plant density, a markedly increased daylength produced a higher level of phenotypes with delayed start of tillering (compare SN conditions at ME and LE).
4.3. End of tillering, competition and growth capacities The dynamics of the cessation of tillering reflected the ways of the onset of competition which occurred in the stands. At LE, some plants stopped tillering early at the beginning of stem elongation while others continued, or some even began to tiller (see 3.3). When the canopy was not closed during stem elongation (Fig. 4), the competition remained very weak for a long time, except locally, among direct neighbours. This is consistent with a situation of reduced growth potential: when the growth without competition is low, the restriction of growth by the same arrangement of neighbours is reduced (results by Lindquist et al., 1994). In the dense stands, the tillering continued late, as in the sparse stands (Table 2). The general onset of competition was not hastened by four times higher plant density, because this density had brought too high proportion of weak phenotypes (WT&T3+ ) (Fig. 5). At SGE, the general cessation of tillering at the beginning of stem elongation was likely due to
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competition for restricted soil resources, because of a sudden drought at that time (Fig. 2). Afterwards, in sparse stands the late closure of the canopy may have allowed for a resumption of tillering — such as in pasture grasses — as a consequence of rains after the drought (Luebs and Laag, 1969). In dense stands, the earlier closure of the canopy prevented the resumption of tillering. In these stands, three times higher plant density caused more weak phenotypes (Fig. 5), but started an earlier onset of competition (Table 2). At ME, the early and definitive cessation of tillering reflected an early establishment of competition between all plants, including the sparse stands, as a result of the high growth potential of the individuals. At ML, the tillering phenotypes seem to be close to those of SGE in sparse stands and to those of LE in dense stands (Fig. 5). In spite of these likely low growth potentials, no significant further tillering was observed (Table 2). Competition must have been established by soil resources restricted by long-lasting drought (Fig. 2).
5. Conclusions In sparse stands, long days at plant emergence highly increased the level of tillering phenotypes with low potentials. That resulted in a delayed markedly onset of competition. The environmental factors usually acting on growth and competition (nitrogen and above all plant density) interacted with daylength on emerging seedlings and modified the phenotype and the growth potential of the plants. As shown through the dynamics of the cessation of tillering, increased plant density, which was expected to compensate for the reduced growth capacities of plants emerging in long days, further reduced these initial growth capacities. Before carrying out the growth, the environmental conditions have differentiated the growth potentials of spring barley plants with the same genotype. When the daylength and the proximity of nearest neighbours interacted, this growth potential was reduced strongly.
Acknowledgements I thank E. Albaret, V. Andre´, G. Bielicki, B. Carette, D. Ezard, J. Hanoteaux, M. Louyot, A. Mante and C. Pravin for their technical assistance, and two anonymous referees for comments on an earlier version of this paper. I am also indebted to Jill Carter for revising the English of the manuscript.
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