Transcriptional landscape of grain development aids researchers in wheat improvement

Published in Ecology & Evolution
Transcriptional landscape of grain development aids researchers in wheat improvement
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Wheat (Triticum spp.), a globally most important and widely cultivated staple food crop,  accounting for nearly 20% of the total calories consumed by humans, in addition, wheat is also more nutritionally balanced for protein, vitamins and minerals than other staple crops (1). Modern wheat production depends on two polyploid species, Triticum aestivum (bread wheat) and Triticum turgidum (var durum), which putatively derived from through natural hybridization and polyploidization of diploid ancestors Triticum  rartu, Aegilops speltoides, and Aegilops tauschii, including domestication, selection and breeding. Historical and recent evidence suggest that T. turgidum (2n = 28, AABB) was derived from a hybridization event happened approximately 0.5 to 3.0 million years ago between an A genome diploid donor (T. monococcum ssp urartu, 2n = 14, AA) and a B genome diploid donor (Ae. speltoides relative, 2n = 14, BB). While the hexaploid wheat (T. aestivum, 2n = 42, AABBDD) arose from an additional polyploidization event occurred about 8000 years ago between a domesticated tetraploid wheat (T. turgidum ssp dicoccum, 2n = 28, AABB) and the D genome diploid wild goat grass (Ae. Tauschii, 2n = 14, DD) (2).
Given its global importance, to increase wheat production by 70% in 2050 to meet the demands of a growing population, researchers and breeders through their collective efforts are working to achieve this challenge. The wheat improvement relies greatly on advanced knowledge and understanding of wheat biology and the molecular basis of key agronomic traits. Recent advances in genomics studies of wheat and its progenitor diploid species led to the generation of draft genome of two diploid progenitors (D genome progenitor Ae. Tauschii and A genome donor, T. urartu) of common wheat were first to be decoded using a shotgun sequencing strategy (3,4). With major efforts from several groups worldwide, more in depth versions of genome sequences of hexaploid wheat (Chinese Spring) were produced and improved with multiple strategies (5,6). Finally, a fully annotated reference genome with a detailed analysis of gene content among subgenomes and the structural organization for all the chromosomes were presents by International Wheat Genome Sequencing Consortium (7). Soon after, the entire genome of durum wheat (DW), which produces pasta, was finished by an international consortium (8). Access to the fully annotated genome sequence in combination with gene expression data not only provides great potential for accelerating the progress of gene discovery underpinning important traits and their breeding, it will also contribute to advancing our understanding of many important biological processes, which include wheat evolution, domestication, polyploidization, as well as genetic and epigenetic interaction between homoeologous genes and genomes.
Wheat yield and quality are determined largely by their grains which consist of three major components: embryo, endosperm and the pericarp (seed coat). The genetic crosstalk between embryo, endosperm, and pericarp tissues during development is highly complex and requires the coordination of several biological processes (9). Gaining access to the transcriptomes of different components of the developing grain offers insight into the biological processes of grain formation. To explore the underpinning gene activities involved in the grain development and characterize the impact of hybridization, polyploidization, and breeding on gene activities during grain development in wheat, we previously performed a comprehensive analysis of global gene expression and alternative splicing (AS) during embryogenesis and grain development in common and durum wheats as well as their three putative diploid ancestors. These studies identified transcriptional signatures and developmental similarities and differences among modern wheat cultivars and their ancestors. Furthermore, the insights gained from these studies revealed the evolutionary divergence of gene expression programs and the contributions of A, B, and D subgenomes to grain development in polyploid wheats. Moreover, we also found that diversity in AS events not only exist between the endosperm, pericarp and embryo overdevelopment, but also between subgenomes. The analysis of AS in homoeologous triads of polyploid wheats revealed evolutionary divergence between gene-level and transcript level regulation of embryogenesis. These findings provide valuable insights into the evolution of gene expression and regulatory features of AS during embryogenesis and grain development in wheat (9,10). 
Hybridization of tetraploid durum wheat (Triticum turgidum ssp. durum; 2n = 4x = 28) and hexaploid bread wheat (Triticum aestivum L.; 2n = 6x = 42) have been used to produce pentaploid hybrids with improved agronomic characters including disease resistance and abiotic stress tolerance (11). These improvements result from genetic diversity associated with the predominance of heterozygous loci in the A and B genomes, together with the retention of a haploid D genome. However, polyploid hybridization between different wheat species can yield incompatibility and sterility issues that challenge trait introgression efforts (12). Global gene expression changes resulting from imbalanced homeolog gene expression and homeolog silencing is a common phenomenon observed in hybridization. The viability of the progeny from interploid crosses depends on the regulation of gene expression from maternal and paternal chromosomes, understanding the effects of merging two regulatory networks into one genetic system on genome wide allelic expression changes in polyploidy species is critical for developing successful interspecific wheat hybrids. To investigate the genome-wide maternal and paternal contributions to polyploid grain development, in this study, we performed a comprehensive gene expression study throughout grain development in the progeny from reciprocal crosses between tetraploid and hexaploid wheat species, with a focus on the reprogramming of gene expression and AS in the embryo. In this study, we found extensive transcriptional changes as well as higher level of AS in pentaploids with a hexaploid mother was observed in reciprocal crosses between hexaploid and tetraploid, which was illustrated by active splicing events, enhanced protein synthesis and chromatin remodeling through biological pathways analysis. We also observed an imbalanced expression pattern of homoeologous genes in pentaploids, with homoeologous gene repressed on the univalent D genome, however, this suppression was attenuated in crosses with a higher ploidy maternal parent. In addition, many more imprinted genes were identified in endosperm and early embryo tissues than previous studies, supporting predominant maternal effects on early embryogenesis (13). 
By systematically investigating the complex transcriptional networks in reciprocal-cross hybrids, this study presents a framework for understanding the genomic incompatibility and transcriptome shock that results from interspecific hybridization and uncovers the transcriptional impacts on hybrid seeds created from agriculturally-relevant polyploid species. These findings, together with the transcriptome resources of embryogenesis and grain development, will help researchers and assist breeders to develop new genetic tools and strategies for exploitation of genetic diversity in wheat and its related species, towards improvements in wheat performance and productivity.  

References

1.    Food and Agriculture Organization of the United Nations, FAOSTAT statistics database, Food balance sheets (2017); www.fao.org/faostat/en/#data/FBS 
2.    El Baidouri M, Murat F, Veyssiere M, et al. Reconciling the evolutionary origin of bread wheat (Triticum aestivum) [J]. New Phytologist, 2017, 213(3): 1477-1486.
3.    Jia J, Zhao S, Kong X, et al. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation[J]. Nature, 2013, 496(7443): 91-95.
4.    Ling H Q, Zhao S, Liu D, et al. Draft genome of the wheat A-genome progenitor Triticum Urartu [J]. Nature, 2013, 496(7443): 87-90.
5.    International Wheat Genome Sequencing Consortium (IWGSC), Mayer K F X, Rogers J, et al. A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome [J]. Science, 2014, 345(6194): 1251788.
6.    Guan J, Garcia D F, Zhou Y, et al. The battle to sequence the bread wheat genome: a tale of the three kingdoms[J]. Genomics, Proteomics & Bioinformatics, 2020, 18(3): 221-229.
7.    International Wheat Genome Sequencing Consortium (IWGSC), Appels R, Eversole K, et al. Shifting the limits in wheat research and breeding using a fully annotated reference genome[J]. Science, 2018, 361(6403): eaar7191. 
8.    Maccaferri M, Harris N S, Twardziok S O, et al. Durum wheat genome highlights past domestication signatures and future improvement targets[J]. Nature genetics, 2019, 51(5): 885-895.
9.    Xiang D, Quilichini T D, Liu Z, et al. The transcriptional landscape of polyploid wheats and their diploid ancestors during embryogenesis and grain development[J]. The Plant Cell, 2019, 31(12): 2888-2911.
10.    Gao P, Quilichini T D, Zhai C, et al. Alternative splicing dynamics and evolutionary divergence during embryogenesis in wheat species[J]. Plant biotechnology journal, 2021, 19(8): 1624-1643.
11.    Han C, Zhang P, Ryan P R, et al. Introgression of genes from bread wheat enhances the aluminium tolerance of durum wheat[J]. Theoretical and Applied Genetics, 2016, 129(4): 729-739.
12.    Lanning S P, Blake N K, Sherman J D, et al. Variable production of tetraploid and hexaploid progeny lines from spring wheat by durum wheat crosses[J]. Crop science, 2008, 48(1): 199-202.
13.    Jia Z, Gao P, Yin F, et al. Asymmetric gene expression in grain development of reciprocal crosses between tetraploid and hexaploid wheats[J]. Communications Biology, 2022, 5(1): 1-15.

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