Sense in sensitivity: difference in the meaning of photoperiod insensitivity between wheat and barley.

The description of long photoperiod sensitivity in wheat and barley is a cause of confusion for researchers working with these crops, usually accustomed to free exchange of physiological and genetic knowledge of such similar crops. Indeed, wheat and barley scientists customarily quote studies of either crop species when researching one of them. Among their numerous similarities, the main gene controlling the long photoperiod sensitivity is the same in both crops (PPD1; PPD-H1 in barley and PPD-D1 in hexaploid wheat). However, the photoperiod responses are different: (i) the main dominant allele inducing shorter time to anthesis is the insensitive allele in wheat (Ppd-D1a) but the sensitive allele in barley (Ppd-H1) (i.e. sensitivity to photoperiod produces opposite effects on time to heading in wheat and barley); (ii) the main 'insensitive' allele in wheat, Ppd-D1a, does confer insensitivity, whilst that of barley reduces the sensitivity but still responds to photoperiod. The different behaviour of PPD1 genes in wheat and barley is put in a common framework based on the similarities and differences of the molecular bases of their mutations, which include polymorphism at gene expression levels, copy number variation, and sequence of coding regions. This common perspective sheds light on a source of confusion for cereal researchers, and prompts us to recommend accounting for the photoperiod sensitivity status of the plant materials when conducting research on genetic control of phenology. Finally, we provide advice to facilitate the management of natural PPD1 diversity in breeding programmes and suggest targets for further modification through gene editing, based on mutual knowledge on the two crops.

Photoperiod sensitivity of Ppd-H1 and ppd-H1 isogenic lines of a spring barley cultivar: exploring extreme photoperiods.

Barley is a long-day plant with a major gene (PPD-H1) that determines its photoperiod sensitivity. Under long days (i.e. 16 h), flowering occurs earlier in sensitive (Ppd-H1) than in insensitive (ppd-H1) genotypes, while under short days (i.e. 12 h) both flower late and more or less simultaneously. We hypothesized that (i) the sensitive line should flower later than the insensitive line under very short days (<12 h), and (ii) both the sensitive and insensitive lines should have similar phenology under very long days (>18 h). When comparing a pair of spring isogenic lines for sensitive and insensitive PPD-H1 alleles (introgressing the PPD-H1 allele into the barley cultivar 'WI4441'), we found responses fully in line with expectations for the commonly explored range from 12 to 16-18 h. When the responses were extended to very short days, sensitivity increased noticeably, and time to flowering of the sensitive line was longer than that of the insensitive one. Under very long days, the sensitive line did not respond further (it seemed to have reached its minimum time to flowering under a 16 h period), while the insensitive line continued shortening its time to flowering until c. 21 h. Consequently, both lines flowered similarly under very long days, which opens opportunities to easily test for differences in earliness per se, as in wheat.

A 'wiring diagram' for sink strength traits impacting wheat yield potential.

Identifying traits for improving sink strength is a bottleneck to increasing wheat yield. The interacting processes determining sink strength and yield potential are reviewed and visualized in a set of 'wiring diagrams', covering critical phases of development (and summarizing known underlying genetics). Using this framework, we reviewed and assembled the main traits determining sink strength and identified research gaps and potential hypotheses to be tested for achieving gains in sink strength. In pre-anthesis, grain number could be increased through: (i) enhanced spike growth associated with optimized floret development and/or a reduction in specific stem-internode lengths and (ii) improved fruiting efficiency through an accelerated rate of floret development, improved partitioning between spikes, or optimized spike cytokinin levels. In post-anthesis, grain, sink strength could be augmented through manipulation of grain size potential via ovary size and/or endosperm cell division and expansion. Prospects for improving spike vascular architecture to support all rapidly growing florets, enabling the improved flow of assimilate, are also discussed. Finally, we considered the prospects for enhancing grain weight realization in relation to genetic variation in stay-green traits as well as stem carbohydrate remobilization. The wiring diagrams provide a potential workspace for breeders and crop scientists to achieve yield gains in wheat and other field crops.

A 'wiring diagram' for source strength traits impacting wheat yield potential.

Source traits are currently of great interest for the enhancement of yield potential; for example, much effort is being expended to find ways of modifying photosynthesis. However, photosynthesis is but one component of crop regulation, so sink activities and the coordination of diverse processes throughout the crop must be considered in an integrated, systems approach. A set of 'wiring diagrams' has been devised as a visual tool to integrate the interactions of component processes at different stages of wheat development. They enable the roles of chloroplast, leaf, and whole-canopy processes to be seen in the context of sink development and crop growth as a whole. In this review, we dissect source traits both anatomically (foliar and non-foliar) and temporally (pre- and post-anthesis), and consider the evidence for their regulation at local and whole-plant/crop levels. We consider how the formation of a canopy creates challenges (self-occlusion) and opportunities (dynamic photosynthesis) for components of photosynthesis. Lastly, we discuss the regulation of source activity by feedback regulation. The review is written in the framework of the wiring diagrams which, as integrated descriptors of traits underpinning grain yield, are designed to provide a potential workspace for breeders and other crop scientists that, along with high-throughput and precision phenotyping data, genetics, and bioinformatics, will help build future dynamic models of trait and gene interactions to achieve yield gains in wheat and other field crops.

The extreme 2016 wheat yield failure in France.

France suffered, in 2016, the most extreme wheat yield decline in recent history, with some districts losing 55% yield. To attribute causes, we combined the largest coherent detailed wheat field experimental dataset with statistical and crop model techniques, climate information, and yield physiology. The 2016 yield was composed of up to 40% fewer grains that were up to 30% lighter than expected across eight research stations in France. The flowering stage was affected by prolonged cloud cover and heavy rainfall when 31% of the loss in grain yield was incurred from reduced solar radiation and 19% from floret damage. Grain filling was also affected as 26% of grain yield loss was caused by soil anoxia, 11% by fungal foliar diseases, and 10% by ear blight. Compounding climate effects caused the extreme yield decline. The likelihood of these compound factors recurring under future climate change is estimated to change with a higher frequency of extremely low wheat yields.

Earliness per se×temperature interaction: consequences on leaf, spikelet, and floret development in wheat.

Wheat adaptation can be fine-tuned by earliness per se (Eps) genes. Although the effects of Eps genes are often assumed to act independently of the environment, previous studies have shown that they exhibit temperature sensitivity. The number of leaves and phyllochron are considered determinants of flowering time and the numerical components of yield include spikelets per spike and fertile floret number within spikelets. We studied the dynamics of leaf, spikelet, and floret development in near isogenic lines with either late or early alleles of Eps-D1 under seven temperature regimes. Leaf appearance dynamics were modulated by temperature, and Eps alleles had a greater effect on the period from flag leaf to heading than phyllochron. In addition, the effects of the Eps alleles on spikelets per spike were minor, and more related to spikelet plastochron than the duration of the early reproductive phase. However, fertile floret number was affected by the interaction between Eps alleles and temperature. So, at 9 °C, Eps-early alleles had more fertile florets than Eps-late alleles, at intermediate temperatures there was no significant difference, and at 18 °C (the highest temperature) the effect was reversed, with lines carrying the late allele producing more fertile florets. These effects were mediated through changes in floret survival; there were no clear effects on the maximum number of floret primordia.

Photoperiod-sensitivity genes shape floret development in wheat.

Lengthening the pre-anthesis period of stem elongation (or late-reproductive phase, LRP) through altering photoperiod sensitivity has been suggested as a potential means to increase the number of fertile florets at anthesis (NFF) in wheat. However, little is known about the effects that the Ppd-1 genes modulating plant response to photoperiod may have on reproductive development. Here, five genotypes with either sensitive (b) or insensitive (a) alleles were grown in chambers under contrasting photoperiods (12 h or 16 h) to assess their effects. The genotypes consisted of the control cultivar Paragon (three Ppd-1b) and four near-isogenic lines of Paragon with Ppd-1a alleles introgressed from: Chinese Spring (Ppd-B1a), GS-100 (Ppd-A1a), Sonora 64 (Ppd-D1a), and Triple Insensitive (three Ppd-1a). Under a 12-h photoperiod, NFF in the genotypes followed the order three Ppd-1b > Ppd-B1a > Ppd-A1a > Ppd-D1a > three Ppd-1a. Under a 16-h photoperiod the differences were milder, but three Ppd-1b still had a greater NFF than the rest. As Ppd-1a alleles shortened the LRP, spikes were lighter and the NFF decreased. The results demonstrated for the first time that Ppd-1a decreases the maximum number of florets initiated through shortening the floret initiation phase, and this partially explained the variations in NFF. The most important impact of Ppd-1a alleles, however, was related to a reduction in survival of floret primordia, which resulted in the lower NFF. These findings reinforce the idea that an increased duration of the LRP, achieved through photoperiod sensitivity, would be useful for increasing wheat yield potential.

Dynamics of floret initiation/death determining spike fertility in wheat as affected by Ppd genes under field conditions.

As wheat yield is linearly related to grain number, understanding the physiological determinants of the number of fertile florets based on floret development dynamics due to the role of the particular genes is relevant. The effects of photoperiod genes on dynamics of floret development are largely ignored. Field experiments were carried out to (i) characterize the dynamics of floret primordia initiation and degeneration and (ii) to determine which are the most critical traits of such dynamics in establishing genotypic differences in the number of fertile florets at anthesis in near isogenic lines (NILs) carrying photoperiod-insensitive alleles. Results varied in magnitude between the two growing seasons, but in general introgression of Ppd-1a alleles reduced the number of fertile florets. The actual effect was affected not only by the genome and the doses but also by the source of the alleles. Differences in the number of fertile florets were mainly explained by differences in the floret generation/degeneration dynamics, and in most cases associated with floret survival. Manipulating photoperiod insensitivity, unquestionably useful for changing flowering time, may reduce spike fertility but much less than proportionally to the change in duration of development, as the insensitivity alleles did increase the rate of floret development.

Effects of ambient temperature in association with photoperiod on phenology and on the expressions of major plant developmental genes in wheat (Triticum aestivum L.).

In addition to its role in vernalization, temperature is an important environmental stimulus in determining plant growth and development. We used factorial combinations of two photoperiods (16H, 12H) and three temperature levels (11, 18 and 25 °C) to study the temperature responses of 19 wheat cultivars with established genetic relationships. Temperature produced more significant effects on plant development than photoperiod, with strong genotypic components. Wheat genotypes with PPD-D1 photoperiod sensitive allele were sensitive to temperature; their development was delayed by higher temperature, which intensified under non-inductive conditions. The effect of temperature on plant development was not proportional; it influenced the stem elongation to the largest extent, and warmer temperature lengthened the lag phase between the detection of first node and the beginning of intensive stem elongation. The gene expression patterns of VRN1, VRN2 and PPD1 were also significantly modified by temperature, while VRN3 was more chronologically regulated. The associations between VRN1 and VRN3 gene expression with early apex development were significant in all treatments but were only significant for later plant developmental phases under optimal conditions (16H and 18 °C). Under 16H, the magnitude of the transient peak expression of VRN2 observed at 18 and 25 °C associated with the later developmental phases.

Genotypic variation in spike fertility traits and ovary size as determinants of floret and grain survival rate in wheat.

Spike fertility traits are critical attributes for grain yield in wheat (Triticum aestivum L.). Here, we examine the genotypic variation in three important traits: maximum number of floret primordia, number of fertile florets, and number of grains. We determine their relationship in determining spike fertility in 30 genotypes grown under two contrasting conditions: field and greenhouse. The maximum number of floret primordia per spikelet (MFS), fertile florets per spikelet (FFS), and number of grains per spikelet (GS) not only exhibited large genotypic variation in both growth conditions and across all spikelet positions studied, but also displayed moderate levels of heritability. FFS was closely associated with floret survival and only weakly related to MFS. We also found that the post-anthesis process of grain set/abortion was important in determining genotypic variation in GS; an increase in GS was mainly associated with improved grain survival. Ovary size at anthesis was associated with both floret survival (pre-anthesis) and grain survival (post-anthesis), and was thus believed to 'connect' the two traits. In this work, proximal florets (i.e. the first three florets from the base of a spikelet: F1, F2, and F3) produced fertile florets and set grains in most cases. The ovary size of more distal florets (F4 and beyond) seemed to act as a decisive factor for grain setting and effectively reflected pre-anthesis floret development. In both growth conditions, GS positively correlated with ovary size of florets in the distal position (F4), suggesting that assimilates allocated to distal florets may play a critical role in regulating grain set.

Variation in developmental patterns among elite wheat lines and relationships with yield, yield components and spike fertility.

Developmental patterns strongly influence spike fertility and grain number, which are primarily determined during the stem elongation period (i.e. time between terminal spikelet phase and anthesis). It has been proposed that the length of the stem elongation phase may, to an extent, affect grain number; thus it would be beneficial to identify genetic variation for the duration of this phase in elite germplasm. Variation in these developmental patterns was studied using 27 elite wheat lines in four experiments across three growing seasons. The results showed that the length of the stem elongation phase was (i) only slightly related to the period from seedling emergence to terminal spikelet, and (ii) more relevant than it for determining time to anthesis. Thus, phenological phases were largely independent and any particular time to anthesis may be reached with different combinations of component phases. Yield components were largely explained by fruiting efficiency of the elite lines used: the relationships were strongly positive and strongly negative with grain number and with grain weight, respectively. Although fruiting efficiency showed a positive trend with the duration of stem elongation that was not significant, a boundary function (which was highly significant) suggests that the length of this phase may impose an upper threshold for fruiting efficiency and grain number, and that maximum values of fruiting efficiency may require a relatively long stem elongation phase.

Agronomic assessment of the wheat semi-dwarfing gene Rht8 in contrasting nitrogen treatments and water regimes.

Reduced height 8 (Rht8) is the main alternative to the GA-insensitive Rht alleles in hot and dry environments where it reduces plant height without yield penalty. The potential of Rht8 in northern-European wheat breeding remains unclear, since the close linkage with the photoperiod-insensitive allele Ppd-D1a is unfavourable in the relatively cool summers. In the present study, two near-isogenic lines (NILs) contrasting for the Rht8/tall allele from Mara in a UK-adapted and photoperiod-sensitive wheat variety were evaluated in trials with varying nitrogen fertiliser (N) treatments and water regimes across sites in the UK and Spain. The Rht8 introgression was associated with a robust height reduction of 11% regardless of N treatment and water regime and the Rht8 NIL was more resistant to root-lodging at agronomically-relevant N levels than the tall NIL. In the UK with reduced solar radiation over the growing season than the site in Spain, the Rht8 NIL showed a 10% yield penalty at standard agronomic N levels due to concomitant reduction in grain number and spike number whereas grain weight and harvest index were not significantly different to the tall NIL. The yield penalty associated with the Rht8 introgression was overcome at low N and in irrigated conditions in the UK, and in the high-temperature site in Spain. Decreased spike length and constant spikelet number in the Rht8 NIL resulted in spike compaction of 15%, independent of N and water regime. The genetic interval of Rht8 overlaps with the compactum gene on 2DS, raising the possibility of the same causative gene. Further genetic dissection of these loci is required.

Critical period for yield determination across grain crops.

Studies across different crops demonstrated that grain or seed number per unit area (GN m-2) is the dominant yield component. Although grains or seeds derive from floret or flower production and survival, the timing of the critical period for GN m-2 determination is known to vary noticeably, from mainly pre-flowering to strongly post-flowering, across major grain crops. Here, we demonstrate that discrepancy between crops in the timing of their critical period is related to the flowering phase duration and the proportion of the whole cycle allocated to pre-flowering development. Changing the perspective, positioning the critical period at the end of the phase when grain abortion occurs instead of flowering, results in the critical period virtually coinciding among contrasting grain crops.

Floret development and grain setting differences between modern durum wheats under contrasting nitrogen availability.

Wheat yield depends on the number of grains per square metre, which in turn is related to the number of fertile florets at anthesis. The dynamics of floret generation/degeneration were studied in contrasting conditions of nitrogen (N) and water availability of modern, well-adapted, durum wheats in order to understand further the bases for grain number determination. Experiments were carried out during the 2008-2009 and 2009-2010 growing seasons at Lleida (NE Spain). The first experiment involved four cultivars (Claudio, Donduro, Simeto, and Vitron) and two contrasting N availabilities (50 kgN ha(-1) and 250 kgN ha(-1); N50 and N250) while experiment 2 included the two cultivars most contrasting in grain setting responsiveness to N in experiment 1, and two levels of N (N50 and N250), under irrigated (IR) and rainfed (RF) conditions. In addition, a detillering treatment was imposed on both cultivars under the IR+N250 condition. The number of fertile florets at anthesis was increased by ~30% in response to N fertilization (averaging across treatments and spikelet positions). The effect of N and water availability was evident on floret developmental rates from the third floret primordium onwards, as these florets in the central spikelets of all genotypes reached the stage of a fertile floret in N250 while in N50 they did not. In this study, clear differences were found between the cultivars in their responsiveness to N by producing more fertile florets at anthesis (through accelerating developmental rates of floret primordia), by increasing the likelihood of particular grains to be set, or by both traits.

Is floret primordia death triggered by floret development in durum wheat?

Survival of floret primordia initiated seems critical for the determination of grain number and yield in wheat, and understanding what determines floret mortality would help in the development of more robust physiological models of yield determination. The growth of the juvenile spikes has been frequently considered the determinant of grain number, implying that floret development would depend on resource availability and that the onset of floret death would be related to spike growth. However, this model has been recently challenged from a study concluding that floret death started when the most advanced floret primordia reached a particular developmental stage. As the few previous studies on this relationship involved photoperiod treatments which affect both floret development and the onset of spike growth, conclusions cannot be considered mechanistic. This comprehensive study analysed in detail floret development in wheat as affected by resource availability (mainly soil nitrogen levels) and found that the onset of floret death may occur when development of the most advanced florets ranged from stages 5 to 9 and that the average and standard deviation of floret developmental stage coinciding with the onset of floret death was not related to the level of availability of resources. These results provide further support to the model relating the onset of floret death with the initiation of active growth of the juvenile spike in which florets are developing.

Awned versus awnless wheat spikes: does it matter?

Awnless and awned wheat is found across the globe. Archeological and historical records show that the wheat spike was predominantly awned across the many millennia following domestication. Thus, ancient farmers did not select against awns at least until the last millennium. Here, we describe the evolution and domestication of wheat awns, quantifying their role in spike photosynthesis and yield under contrasting environments. Awns increase grain weight directly (increasing the size of all grains) or indirectly (increasing the failure of distal grains), but not as a consequence of additional spike photosynthesis. However, a trade-off is produced through decreasing grain number. Thus, favorable effects of awns on yield are not consistently found across environments.

Wheat floret survival as related to pre-anthesis spike growth.

Further improvements to wheat yield potential will be essential to meet future food demand. As yield is related to the number of fertile florets and grains, an understanding of the basis of their generation is instrumental to raising yield. Based on (i) a strong positive association between the number of fertile florets or grains and spike dry weight at anthesis; and (ii) the finding that floret death occurs when spikes grow at maximum rate, it was always assumed that floret survival depends on the growth of the spike. However, this assumption was recently questioned, suggesting that assimilates diverted to the spike do not determine the number of florets and grains and that the onset of floret death may instead be a developmental process that is not associated with spike growth. In this study, the relationships between the fate of floret primordia and spike growth from six independent experiments that included different growing conditions (greenhouse/field experiments, growing seasons, photoperiod/shading treatments during the floret primordia phase) and diverse cultivar types (winter/spring, semi-dwarf/standard-height, photoperiod sensitive/insensitive) were re-analysed together. Onset of floret death was associated with the beginning of spike growth at the maximum rate in c. 80% of the cases analysed; and the rate of floret death (the main determinant of floret survival) showed a negative quantitative relationship with spike weight at anthesis. As floret death and survival were shown to be linked to pre-anthesis spike growth, the strategy of focusing on traits associated with pre-anthesis spike growth when breeding to increase wheat yield potential further is valuable.

Raising yield potential of wheat. III. Optimizing partitioning to grain while maintaining lodging resistance.

A substantial increase in grain yield potential is required, along with better use of water and fertilizer, to ensure food security and environmental protection in future decades. For improvements in photosynthetic capacity to result in additional wheat yield, extra assimilates must be partitioned to developing spikes and grains and/or potential grain weight increased to accommodate the extra assimilates. At the same time, improvement in dry matter partitioning to spikes should ensure that it does not increase stem or root lodging. It is therefore crucial that improvements in structural and reproductive aspects of growth accompany increases in photosynthesis to enhance the net agronomic benefits of genetic modifications. In this article, six complementary approaches are proposed, namely: (i) optimizing developmental pattern to maximize spike fertility and grain number, (ii) optimizing spike growth to maximize grain number and dry matter harvest index, (iii) improving spike fertility through desensitizing floret abortion to environmental cues, (iv) improving potential grain size and grain filling, and (v) improving lodging resistance. Since many of the traits tackled in these approaches interact strongly, an integrative modelling approach is also proposed, to (vi) identify any trade-offs between key traits, hence to define target ideotypes in quantitative terms. The potential for genetic dissection of key traits via quantitative trait loci analysis is discussed for the efficient deployment of existing variation in breeding programmes. These proposals should maximize returns in food production from investments in increased crop biomass by increasing spike fertility, grain number per unit area and harvest index whilst optimizing the trade-offs with potential grain weight and lodging resistance.

Wheat Developmental Traits as Affected by the Interaction between Eps-7D and Temperature under Contrasting Photoperiods with Insensitive Ppd-D1 Background.

Earliness per se (Eps) genes are important to fine tune adaptation, and studying their probable pleiotropic effect on wheat yield traits is worthwhile. In addition, it has been shown that some Eps genes interact with temperature and therefore determining the likely Eps × temperature interaction is needed for each newly identified Eps gene. We studied two NILs differing in the newly identified Eps-7D (carrying insensitive Ppd-D1 in the background) under three temperature regimes (9, 15 and 18 °C) and two photoperiods (12 and 24 h). Eps-7D affected time to anthesis as expected and the Eps-7D-late allele extended both the period before and after terminal spikelet. The interaction effect of Eps-7D × temperature was significant but not cross-over: the magnitude and level of significance of the difference between NILs with the late or early allele was affected by the growing temperature (i.e., difference was least at 18 °C and largest at 9 °C), and the differences caused due to temperature sensitivity were influenced by photoperiod. The rate of leaf initiation was faster in NIL with Eps-7D-early than with the late allele which compensated for the shorter duration of leaf initiation resulting in similar final leaf number between two NILs. Eps-7D-late consistently increased spike fertility through improving floret primordia survival as a consequence of extending the late reproductive phase.

Phenology and Floret Development as Affected by the Interaction between Eps-7D and Ppd-D1.

Earliness per se (Eps) genes may play a critical role in further improving wheat adaptation and fine-tuning wheat development to cope with climate change. There are only few studies on the detailed effect of Eps on wheat development and fewer on the interaction of Eps with the environment and other genes determining time to anthesis. Furthermore, it seems relevant to study every newly discovered Eps gene and its probable interactions as the mechanisms and detailed effects of each Eps may be quite different. In the present study, we evaluated NILs differing in the recently identified Eps-7D as well as in Ppd-D1 at three temperature regimes (9, 15 and 18 °C) under short day. The effect of Eps-7D on time to anthesis as well as on its component phases varied both qualitatively and quantitatively depending on the allelic status of Ppd-D1 and temperature, being larger in a photoperiod-sensitive background. A more noticeable effect of Eps-7D (when combined with Ppd-D1b) was realised during the late reproductive phase. Consequently, the final leaf number was not clearly altered by Eps-7D, while floret development of the labile florets (florets 2 and 3 in this case, depending on the particular spikelet) was favoured by the action of the Eps-7D-late allele, increasing the likelihood of particular florets to become fertile, and consequently, improving spike fertility when combined with Ppd-D1b.