Photoperiod-1 regulates the wheat inflorescence transcriptome to influence spikelet architecture and flowering time.

Photoperiod insensitivity has been selected by breeders to help adapt crops to diverse environments and farming practices. In wheat, insensitive alleles of Photoperiod-1 (Ppd-1) relieve the requirement of long daylengths to flower by promoting expression of floral promoting genes early in the season; however, these alleles also limit yield by reducing the number and fertility of grain-producing florets through processes that are poorly understood. Here, we performed transcriptome analysis of the developing inflorescence using near-isogenic lines that contain either photoperiod-insensitive or null alleles of Ppd-1, during stages when spikelet number is determined and floret development initiates. We report that Ppd-1 influences the stage-specific expression of genes with roles in auxin signaling, meristem identity, and protein turnover, and analysis of differentially expressed transcripts identified bZIP and ALOG transcription factors, namely PDB1 and ALOG1, which regulate flowering time and spikelet architecture. These findings enhance our understanding of genes that regulate inflorescence development and introduce new targets for improving yield potential.

Finding the right balance: The enduring role of florigens during cereal inflorescence development and their influence on fertility.

Flowering is a vital process in a plant's lifecycle and variation for flowering-time has helped cereals adapt to diverse environments. Much cereal research has focused on understanding how flowering signals, or florigens, regulate the floral transition and timing of ear emergence. However, flowering genes also perform an enduring role during inflorescence development, with genotypes that elicit a weaker flowering signal producing more elaborately branched inflorescences with extra floret-bearing spikelets. While this outcome indicates that variable expression of flowering genes could boost yield potential, further analysis has shown that dampened florigen levels can compromise fertility, negating the benefit of extra grain-producing sites. Here, we discuss ways that florigens contribute to early and late inflorescence development, including their influence on branch/spikelet architecture and fertility. We propose that a deeper understanding of the role for florigens during inflorescence development could be used to balance the effects of florigens throughout flowering to improve productivity.

Widespread incomplete lineage sorting and introgression shaped adaptive radiation in the Gossypium genus.

Cotton (Gossypium) stands as a crucial economic crop, serving as the primary source of natural fiber for the textile sector. However, the evolutionary mechanisms driving speciation within the Gossypium genus remain unresolved. In this investigation, we leveraged 25 Gossypium genomes and introduced four novel assemblies-G. harknessii, G. gossypioides, G. trilobum, and G. klotzschianum (Gklo)-to delve into the speciation history of this genus. Notably, we encountered intricate phylogenies potentially stemming from introgression. These complexities are further compounded by incomplete lineage sorting (ILS), a factor likely to have been instrumental in shaping the swift diversification of cotton. Our focus subsequently shifted to the rapid radiation episode during a concise period in Gossypium evolution. For a recently diverged lineage comprising G. davidsonii, Gklo, and G. raimondii, we constructed a finely detailed ILS map. Intriguingly, this analysis revealed the non-random distribution of ILS regions across the reference Gklo genome. Moreover, we identified signs of robust natural selection influencing specific ILS regions. Noteworthy variations pertaining to speciation emerged between the closely related sister species Gklo and G. davidsonii. Approximately 15.74% of speciation structural variation genes and 12.04% of speciation-associated genes were estimated to intersect with ILS signatures. These findings enrich our understanding of the role of ILS in adaptive radiation, shedding fresh light on the intricate speciation history of the Gossypium genus.

Challenges facing sustainable protein production: Opportunities for cereals.

Rising demands for protein worldwide are likely to drive increases in livestock production, as meat provides ∼40% of dietary protein. This will come at a significant environmental cost, and a shift toward plant-based protein sources would therefore provide major benefits. While legumes provide substantial amounts of plant-based protein, cereals are the major constituents of global foods, with wheat alone accounting for 15-20% of the required dietary protein intake. Improvement of protein content in wheat is limited by phenotyping challenges, lack of genetic potential of modern germplasms, negative yield trade-offs, and environmental costs of nitrogen fertilizers. Presenting wheat as a case study, we discuss how increasing protein content in cereals through a revised breeding strategy combined with robust phenotyping could ensure a sustainable protein supply while minimizing the environmental impact of nitrogen fertilizer.

Reviving grain quality in wheat through non-destructive phenotyping techniques like hyperspectral imaging.

A long-term goal of breeders and researchers is to develop crop varieties that can resist environmental stressors and produce high yields. However, prioritising yield often compromises improvement of other key traits, including grain quality, which is tedious and time-consuming to measure because of the frequent involvement of destructive phenotyping methods. Recently, non-destructive methods such as hyperspectral imaging (HSI) have gained attention in the food industry for studying wheat grain quality. HSI can quantify variations in individual grains, helping to differentiate high-quality grains from those of low quality. In this review, we discuss the reduction of wheat genetic diversity underlying grain quality traits due to modern breeding, key traits for grain quality, traditional methods for studying grain quality and the application of HSI to study grain quality traits in wheat and its scope in breeding. Our critical review of literature on wheat domestication, grain quality traits and innovative technology introduces approaches that could help improve grain quality in wheat.

Advancing understanding of oat phenology for crop adaptation.

Oat (Avena sativa) is an annual cereal grown for forage, fodder and grain. Seasonal flowering behaviour, or phenology, is a key contributor to the success of oat as a crop. As a species, oat is a vernalization-responsive long-day plant that flowers after winter as days lengthen in spring. Variation in both vernalization and daylength requirements broadens adaptation of oat and has been used to breed modern cultivars with seasonal flowering behaviours suited to different regions, sowing dates and farming practices. This review examines the importance of variation in oat phenology for crop adaptation. Strategies to advance understanding of the genetic basis of oat phenology are then outlined. These include the potential to transfer knowledge from related temperate cereals, particularly wheat (Triticum aestivum) and barley (Hordeum vulgare), to provide insights into the potential molecular basis of variation in oat phenology. Approaches that use emerging genomic resources to directly investigate the molecular basis of oat phenology are also described, including application of high-resolution genome-wide diversity surveys to map genes linked to variation in flowering behaviour. The need to resolve the contribution of individual phenology genes to crop performance by developing oat genetic resources, such as near-isogenic lines, is emphasised. Finally, ways that deeper knowledge of oat phenology can be applied to breed improved varieties and to inform on-farm decision-making are outlined.

A scalable phenotyping approach for female floral organ development and senescence in the absence of pollination in wheat.

In the absence of pollination, female reproductive organs senesce, leading to an irrevocable loss in the reproductive potential of the flower, which directly affects seed set. In self-pollinating crops like wheat (Triticum aestivum), the post-anthesis viability of unpollinated carpels has been overlooked, despite its importance for hybrid seed production systems. To advance our knowledge of carpel development in the absence of pollination, we created a high-throughput phenotyping approach to quantify stigma and ovary morphology. We demonstrate the suitability of the approach, which uses light-microscopy imaging and machine learning, for the analysis of floral organ traits in field-grown plants using fresh and fixed samples. We show that the unpollinated carpel undergoes a well-defined initial growth phase, followed by a peak phase in which stigma area reaches its maximum and the radial expansion of the ovary slows, and a final deterioration phase. These developmental dynamics were consistent across years and could be used to classify male-sterile cultivars. This phenotyping approach provides a new tool for examining carpel development, which we hope will advance research into female fertility of wheat.

MicroRNA-resistant alleles of HOMEOBOX DOMAIN-2 modify inflorescence branching and increase grain protein content of wheat.

Plant and inflorescence architecture determine the yield potential of crops. Breeders have harnessed natural diversity for inflorescence architecture to improve yields, and induced genetic variation could provide further gains. Wheat is a vital source of protein and calories; however, little is known about the genes that regulate the development of its inflorescence. Here, we report the identification of semidominant alleles for a class III homeodomain-leucine zipper transcription factor, HOMEOBOX DOMAIN-2 (HB-2), on wheat A and D subgenomes, which generate more flower-bearing spikelets and enhance grain protein content. These alleles increase HB-2 expression by disrupting a microRNA 165/166 complementary site with conserved roles in plants; higher HB-2 expression is associated with modified leaf and vascular development and increased amino acid supply to the inflorescence during grain development. These findings enhance our understanding of genes that control wheat inflorescence development and introduce an approach to improve the nutritional quality of grain.

Population genomic analysis of Aegilops tauschii identifies targets for bread wheat improvement.

Aegilops tauschii, the diploid wild progenitor of the D subgenome of bread wheat, is a reservoir of genetic diversity for improving bread wheat performance and environmental resilience. Here we sequenced 242 Ae. tauschii accessions and compared them to the wheat D subgenome to characterize genomic diversity. We found that a rare lineage of Ae. tauschii geographically restricted to present-day Georgia contributed to the wheat D subgenome in the independent hybridizations that gave rise to modern bread wheat. Through k-mer-based association mapping, we identified discrete genomic regions with candidate genes for disease and pest resistance and demonstrated their functional transfer into wheat by transgenesis and wide crossing, including the generation of a library of hexaploids incorporating diverse Ae. tauschii genomes. Exploiting the genomic diversity of the Ae. tauschii ancestral diploid genome permits rapid trait discovery and functional genetic validation in a hexaploid background amenable to breeding.

Evolution: Replicated mutation of COL2 contributed long-day flowering in common bean.

The ability to flower without strict daylength constraints has helped spread cultivation of crop plants to new locations. The generation of daylength-insensitive common bean accessions in central and South America involved the repeated selection of mutant alleles for a key transcription factor that suppresses long-day flowering.

Stepwise increases in FT1 expression regulate seasonal progression of flowering in wheat (Triticum aestivum).

Flowering is regulated by genes that respond to changing daylengths and temperature, which have been well studied using controlled conditions; however, the molecular processes underpinning flowering in nature remain poorly understood. Here, we investigate the genetic pathways that coordinate flowering and inflorescence development of wheat (Triticum aestivum) as daylengths extend naturally in the field, using lines that contain variant alleles for the key photoperiod gene, Photoperiod-1 (Ppd-1). We found flowering involves a stepwise increase in the expression of FLOWERING LOCUS T1 (FT1), which initiates under day-neutral conditions of early spring. The incremental rise in FT1 expression is overridden in plants that contain a photoperiod-insensitive allele of Ppd-1, which hastens the completion of spikelet development and accelerates flowering time. The accelerated inflorescence development of photoperiod-insensitive lines is promoted by advanced seasonal expression of floral meristem identity genes. The completion of spikelet formation is promoted by FLOWERING LOCUS T2, which regulates spikelet number and is activated by Ppd-1. In wheat, flowering under natural photoperiods is regulated by stepwise increases in the expression of FT1, which responds dynamically to extending daylengths to promote early inflorescence development. This research provides a strong foundation to improve yield potential by fine-tuning the photoperiod-dependent control of inflorescence development.

Multi-parent populations in crops: a toolbox integrating genomics and genetic mapping with breeding.

Crop populations derived from experimental crosses enable the genetic dissection of complex traits and support modern plant breeding. Among these, multi-parent populations now play a central role. By mixing and recombining the genomes of multiple founders, multi-parent populations combine many commonly sought beneficial properties of genetic mapping populations. For example, they have high power and resolution for mapping quantitative trait loci, high genetic diversity and minimal population structure. Many multi-parent populations have been constructed in crop species, and their inbred germplasm and associated phenotypic and genotypic data serve as enduring resources. Their utility has grown from being a tool for mapping quantitative trait loci to a means of providing germplasm for breeding programmes. Genomics approaches, including de novo genome assemblies and gene annotations for the population founders, have allowed the imputation of rich sequence information into the descendent population, expanding the breadth of research and breeding applications of multi-parent populations. Here, we report recent successes from crop multi-parent populations in crops. We also propose an ideal genotypic, phenotypic and germplasm 'package' that multi-parent populations should feature to optimise their use as powerful community resources for crop research, development and breeding.

Feeling the heat: developmental and molecular responses of wheat and barley to high ambient temperatures.

The increasing demand for global food security in the face of a warming climate is leading researchers to investigate the physiological and molecular responses of cereals to rising ambient temperatures. Wheat and barley are temperate cereals whose yields are adversely affected by high ambient temperatures, with each 1 °C increase above optimum temperatures reducing productivity by 5-6%. Reproductive development is vulnerable to high-temperature stress, which reduces yields by decreasing grain number and/or size and weight. In recent years, analysis of early inflorescence development and genetic pathways that control the vegetative to floral transition have elucidated molecular processes that respond to rising temperatures, including those involved in the vernalization- and photoperiod-dependent control of flowering. In comparison, our understanding of genes that underpin thermal responses during later developmental stages remains poor, thus highlighting a key area for future research. This review outlines the responses of developmental genes to warmer conditions and summarizes our knowledge of the reproductive traits of wheat and barley influenced by high temperatures. We explore ways in which recent advances in wheat and barley research capabilities could help identify genes that underpin responses to rising temperatures, and how improved knowledge of the genetic regulation of reproduction and plant architecture could be used to develop thermally resilient cultivars.

TEOSINTE BRANCHED1 regulates height and stem internode length in bread wheat.

Regulation of plant height and stem elongation has contributed significantly to improvement of cereal productivity by reducing lodging and improving distribution of assimilates to the inflorescence and grain. In wheat, genetic control of height has been largely contributed by the Reduced height-1 alleles that confer gibberellin insensitivity; the beneficial effects of these alleles are associated with less favourable effects involving seedling emergence, grain quality, and inflorescence architecture that have driven new research investigating genetic variation of stem growth. Here, we show that TEOSINTE BRANCHED1 (TB1) regulates height of wheat, with TB1 being expressed at low levels in nodes of the main culm prior to elongation, and increased dosage of TB1 restricting elongation of stem internodes. The effect of TB1 on stem growth is not accompanied by poor seedling emergence, as transgenic lines with increased activity of TB1 form longer coleoptiles than null transgenic controls. Analysis of height in a multiparent mapping population also showed that allelic variation for TB1 on the B genome influences height, with plants containing the variant TB-B1b allele being taller than those with the wild-type TB-B1a allele. Our results show that TB1 restricts height and stem elongation in wheat, suggesting that variant alleles that alter the expression or function of TB1 could be used as a new source of genetic diversity for optimizing architecture of wheat in breeding programmes.

VERNALIZATION1 controls developmental responses of winter wheat under high ambient temperatures.

Low temperatures are required to regulate the transition from vegetative to reproductive growth via a pathway called vernalization. In wheat, vernalization predominantly involves the cold upregulation of the floral activator VERNALIZATION1 (VRN1). Here, we have used an extreme vernalization response, identified through studying ambient temperature responses, to reveal the complexity of temperature inputs into VRN-A1, with allelic inter-copy variation at a gene expansion of VRN-A1 modulating these effects. We find that the repressors of the reproductive transition, VERNALIZATION2 (VRN2) and ODDSOC2, are re-activated when plants experience high temperatures during and after vernalization. In addition, this re-activation is regulated by photoperiod for VRN2 but was independent of photoperiod for ODDSOC2 We also find this warm temperature interruption affects flowering time and floret number and is stage specific. This research highlights the important balance between floral activators and repressors in coordinating the response of a plant to temperature, and that the absence of warmth is essential for the completion of vernalization. This knowledge can be used to develop agricultural germplasm with more predictable vernalization responses that will be more resilient to variable growth temperatures.

How can developmental biology help feed a growing population?

Agriculture is challenged globally from a variety of fronts, including a steady increase in world population, changes in climate and a requirement to reduce fertiliser inputs. In the production of crops that are able to overcome these challenges, developmental biology can play a crucial role. The process of domesticating wild progenitors into edible crops is closely linked to modification of developmental processes, and the steps that are needed to face the current challenges will equally require developmental modifications. In this Spotlight, we describe the achievements by developmental biologists in identifying the genes responsible for domestication of some of the most important crops, and highlight that developmental biology is in a unique position to remain centre stage in improving crop performance to meet current and future demands. We propose that the explosive technological advances in sequencing, genome editing and advanced data processing provide an excellent opportunity for researchers to combine scientific disciplines and realise the continued potential of plants as the primary food source for generations to come.

Genetic pathways controlling inflorescence architecture and development in wheat and barley.

Modifications of inflorescence architecture have been crucial for the successful domestication of wheat and barley, which are central members of the Triticeae tribe that provide essential grains for the human diet. Investigation of the genes and alleles that underpin domestication-related traits has provided valuable insights into the molecular regulation of inflorescence development of the Triticeae, and further investigation of modified forms of architecture are proving to be equally fruitful. The identified genes are involved in diverse biological processes, including transcriptional regulation, hormone biosynthesis and metabolism, post-transcriptional and post-translational regulation, which alter inflorescence architecture by modifying the development and fertility of lateral organs, called spikelets and florets. Recent advances in sequencing capabilities and the generation of mutant populations are accelerating the identification of genes that influence inflorescence development, which is important given that genetic variation for this trait promises to be a valuable resource for optimizing grain production. This review assesses recent advances in our understanding of the genes controlling inflorescence development in wheat and barley, with the aim of highlighting the importance of improvements in developmental biology for optimizing the agronomic performance of staple crop plants.

Zebularine treatment is associated with deletion of FT-B1 leading to an increase in spikelet number in bread wheat.

The number of rachis nodes (spikelets) on a wheat spike is a component of grain yield that correlates with flowering time. The genetic basis regulating flowering in cereals is well understood, but there are reports that flowering time can be modified at a high frequency by selective breeding, suggesting that it may be regulated by both epigenetic and genetic mechanisms. We investigated the role of DNA methylation in regulating spikelet number and flowering time by treating a semi-spring wheat with the demethylating agent, Zebularine. Three lines with a heritable increase in spikelet number were identified. The molecular basis for increased spikelet number was not determined in 2 lines, but the phenotype showed non-Mendelian inheritance, suggesting that it could have an epigenetic basis. In the remaining line, the increased spikelet phenotype behaved as a Mendelian recessive trait and late flowering was associated with a deletion encompassing the floral promoter, FT-B1. Deletion of FT-B1 delayed the transition to reproductive growth, extended the duration of spike development, and increased spikelet number under different temperature regimes and photoperiod. Transiently disrupting DNA methylation can generate novel flowering behaviour in wheat, but these changes may not be sufficiently stable for use in breeding programs.