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.

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.

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.

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.

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.

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.

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.

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.

Addressing Research Bottlenecks to Crop Productivity.

Asymmetry of investment in crop research leads to knowledge gaps and lost opportunities to accelerate genetic gain through identifying new sources and combinations of traits and alleles. On the basis of consultation with scientists from most major seed companies, we identified several research areas with three common features: (i) relatively underrepresented in the literature; (ii) high probability of boosting productivity in a wide range of crops and environments; and (iii) could be researched in 'precompetitive' space, leveraging previous knowledge, and thereby improving models that guide crop breeding and management decisions. Areas identified included research into hormones, recombination, respiration, roots, and source-sink, which, along with new opportunities in phenomics, genomics, and bioinformatics, make it more feasible to explore crop genetic resources and improve breeding strategies.

Interactions between two QTLs for time to anthesis on spike development and fertility in wheat.

Earliness per se (Eps) genes are reported to be important in fine-tuning flowering time in wheat independently of photoperiod (Ppd) and vernalisation (Vrn). Unlike Ppd and Vrn genes, Eps have relatively small effects and their physiological effect along with chromosomal position are not well defined. We evaluated eight lines derived from crossing two vernalisation insensitive lines, Paragon and Baj (late and early flowering respectively), to study the detailed effects of two newly identified QTLs, Eps-7D and Eps-2B and their interactions under field conditions. The effect of both QTLs was minor and was affected by the allelic status of the other. While the magnitude of effect of these QTLs on anthesis was similar, they are associated with very different profiles of pre-anthesis development which also depends on their interaction. Eps-7D affected both duration before and after terminal spikelet while not affecting final leaf number (FLN) so Eps-7D-early had a faster rate of leaf appearance. Eps-2B acted more specifically in the early reproductive phase and slightly altered FLN without affecting the leaf appearance rate. Both QTLs affected the spike fertility by altering the rate of floret development and mortality. The effect of Eps-2B was very small but consistent in that -late allele tended to produce more fertile florets.

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.

Earliness Per Se by Temperature Interaction on Wheat Development.

Differences in time to heading that remain after photoperiod and vernalisation requirements have been saturated are classified as earliness per se (Eps) effects. It has been commonly assumed that Eps genes are purely constitutive and independent of environment, although the likely effect of temperature on Eps effects in hexaploid wheat has never been tested. We grew four near isogenic lines (NILs) for the Eps gene located in chromosome 1D (Eps-D1) at 6, 9, 12, 15, 18, 21 and 24 °C. In line with expectations we found that lines carrying the Eps-late allele were always later than those with Eps-early alleles. But in addition, we reported for the first time that the magnitude of the effect increased with decreasing temperature: an Eps x temperature interaction in hexaploid wheat. Variation in heading time due to Eps x temperature was associated with an increase in sensitivity to temperature mainly during late reproductive phase. Moreover, we showed that Eps alleles exhibited differences in cardinal (base, optimum, maximum) temperatures and that the expression of ELF3, (the likely candidate for Eps-D1) also interacted with temperature.

Physiological Basis of Genotypic Response to Management in Dryland Wheat.

A great majority of dryland wheat producers are reluctant to intensify management due to the assumption that lack of water availability is the most critical factor limiting yield and thus, the response to management intensification would be limited. We conducted on-farm field experiments across three locations and two growing seasons in Kansas using 21 modern winter wheat genotypes grown under either standard (SM) or intensified management (IM) systems. The goals of this study were to (i) determine whether the SM adopted is adequate to reach achievable yields by farmers in the region and (ii) identify differences in responsiveness to IM among a range of modern genotypes. Across all sites-years and genotypes, the IM increased yield by 0.9 Mg ha-1, outyielding the SM system even in the lowest yielding conditions. As expected, the yield response to IM increased with the achievable yield of the environment and genotype. Across all sources of variation, the yield responsiveness to IM was related to increased biomass rather than harvest index, strongly driven by improvements in grain number (and independent of changes in grain weight), and by improvements in N uptake which resulted from greater biomass and shoot N concentration. The IM system generally also increased grain N concentration and decreased the grain N dilution effect from increased yield. Genotypes varied in their response to IM, with major response patterns resulting from the combination of response magnitude (large vs. small) and consistency (variable vs. consistent). Genotypes with high mean response and high variability in the response to IM across years could offer greater opportunities for producers to maximize yield as those genotypes showed greater yield gain from IM when conditions favored their response. For the background conditions evaluated, intensifying management could improve wheat yield in between c. 0.2 and 1.5 Mg ha-1 depending on genotype.

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.

Can N management affect the magnitude of yield loss due to heat waves in wheat and maize?

Deleterious effects of heat on crop yields are well documented and the occurrence of heat stresses will likely be a major constraint to achieving increased yields of major crops. Thus, agronomic and genetic strategies for increased resilience to high temperatures will be necessary. Much of the work done on this area has been focused to identify genetic sources of increased resilience and much less has been done on the crop ecology side. Nitrogen (N) fertilization is within the most common management practices used in cereal production, however, there have been limited efforts to elucidate to what degree the level of soil fertility may affect the magnitude of the high temperature effect on crop yield. The likely interaction may be relevant for designing more appropriate fertilization strategies. We conducted different studies on maize (2009-2012) and wheat (2012-2013), always under field conditions, to determine whether the availability of N may be responsible for the magnitude of the yield penalty imposed by heat stress during reproductive phases (i.e. when heat waves are more likely). We concluded that sensitivity to heat stress increased with increasing N availability and speculated that moderate N stress might produce in the crop plants a sort of acclimation to reduce sensitivity to other stresses. Fertilisation recommendations in the future may need to balance the yielding benefits of high N availability with the detrimental effect of increasing sensitivity to heat stress.

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.

Wheat pre-anthesis development as affected by photoperiod sensitivity genes (Ppd-1) under contrasting photoperiods.

Fine tuning wheat phenology is of paramount importance for adaptation. A better understanding of how genetic constitution modulates the developmental responses during pre-anthesis phases would help to maintain or even increase yield potential as temperature increases due to climate change. The photoperiod-sensitive cultivar Paragon, and four near isogenic lines with different combinations of insensitivity alleles (Ppd-A1a, Ppd-B1a, Ppd-D1a or their triple stack) were evaluated under short (12h) and long (16h) photoperiods. Insensitivity alleles decreased time to anthesis and duration of the three pre-anthesis phases (vegetative, early reproductive and late reproductive), following the Ppd-D1a > Ppd-A1a > Ppd-B1a ranking of strength. Stacking them intensified the insensitivity, but had no additive effect over that of Ppd-D1a. The late reproductive phase was the most responsive, even exhibiting a qualitative response. Leaf plastochron was not affected but spikelet plastochron increased according to Ppd-1a ranking of strength. Earlier anthesis resulted from less leaves differentiated and a fine tuning effect of accelerated rate of leaf appearance. None of the alleles affected development exclusively during any particular pre-anthesis phase, which would be ideal for tailoring time to anthesis with specific partitioning of developmental time into particular phases. Other allelic variants should be further tested to this purpose.

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.

A carotenogenic mini-pathway introduced into white corn does not affect development or agronomic performance.

High-carotenoid corn (Carolight®) has been developed as a vehicle to deliver pro-vitamin A in the diet and thus address vitamin A deficiency in at-risk populations in developing countries. Like any other novel crop, the performance of Carolight® must be tested in different environments to ensure that optimal yields and productivity are maintained, particularly in this case to ensure that the engineered metabolic pathway does not attract a yield penalty. Here we compared the performance of Carolight® with its near isogenic white corn inbred parental line under greenhouse and field conditions, and monitored the stability of the introduced trait. We found that Carolight® was indistinguishable from its near isogenic line in terms of agronomic performance, particularly grain yield and its main components. We also established experimentally that the functionality of the introduced trait was indistinguishable when plants were grown in a controlled environment or in the field. Such thorough characterization under different agronomic conditions is rarely performed even for first-generation traits such as herbicide tolerance and pest resistance, and certainly not for complex second-generation traits such as the metabolic remodeling in the Carolight® variety. Our results therefore indicate that Carolight® can now be incorporated into breeding lines to generate hybrids with locally adapted varieties for further product development and assessment.