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Asymmetric gene expression in grain development of reciprocal crosses between tetraploid and hexaploid wheats.

ABSTRACT: Production of viable progeny from interploid crosses requires precise regulation of gene expression from maternal and paternal chromosomes, yet the transcripts contributed to hybrid seeds from polyploid parent species have rarely been explored. To investigate the genome-wide maternal and paternal contributions to polyploid grain development, we analyzed the transcriptomes of developing embryos, from zygote to maturity, alongside endosperm in two stages of development, using reciprocal crosses between tetraploid and hexaploid wheats. Reciprocal crosses between species with varied levels of ploidy displayed broad impacts on gene expression, including shifts in alternative splicing events in select crosses, as illustrated by active splicing events, enhanced protein synthesis and chromatin remodeling. Homoeologous gene expression was repressed on the univalent D genome in pentaploids, but this suppression was attenuated in crosses with a higher ploidy maternal parent. Imprinted genes were identified in endosperm and early embryo tissues, supporting predominant maternal effects on early embryogenesis. 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.

SUBMITTER: Jia Z

PROVIDER: S-EPMC9789062 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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Asymmetric gene expression in grain development of reciprocal crosses between tetraploid and hexaploid wheats.

Jia Zhen Z Gao Peng P Yin Feifan F Quilichini Teagen D TD Sheng Huajin H Song Jingpu J Yang Hui H Gao Jie J Chen Ting T Yang Bo B Kochian Leon V LV Zou Jitao J Patterson Nii N Yang Qingyong Q Gillmor C Stewart CS Datla Raju R Li Qiang Q Xiang Daoquan D

Communications biology 20221223 1

Production of viable progeny from interploid crosses requires precise regulation of gene expression from maternal and paternal chromosomes, yet the transcripts contributed to hybrid seeds from polyploid parent species have rarely been explored. To investigate the genome-wide maternal and paternal contributions to polyploid grain development, we analyzed the transcriptomes of developing embryos, from zygote to maturity, alongside endosperm in two stages of development, using reciprocal crosses be ...[more]

PMID: 36564439

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Project description:BACKGROUND: Grain size and shape greatly influence grain weight which ultimately enhances grain yield in wheat. Digital imaging (DI) based phenomic characterization can capture the three dimensional variation in grain size and shape than has hitherto been possible. In this study, we report the results from using digital imaging of grain size and shape to understand the relationship among different components of this trait, their contribution to enhance grain weight, and to identify genomic regions (QTLs) controlling grain morphology using genome wide association mapping with high density diversity array technology (DArT) and allele-specific markers. RESULTS: Significant positive correlations were observed between grain weight and grain size measurements such as grain length (r?=?0.43), width, thickness (r?=?0.64) and factor from density (FFD) (r?=?0.69). A total of 231 synthetic hexaploid wheats (SHWs) were grouped into five different sub-clusters by Bayesian structure analysis using unlinked DArT markers. Linkage disequilibrium (LD) decay was observed among DArT loci?>?10 cM distance and approximately 28% marker pairs were in significant LD. In total, 197 loci over 60 chromosomal regions and 79 loci over 31 chromosomal regions were associated with grain morphology by genome wide analysis using general linear model (GLM) and mixed linear model (MLM) approaches, respectively. They were mainly distributed on homoeologous group 2, 3, 6 and 7 chromosomes. Twenty eight marker-trait associations (MTAs) on the D genome chromosomes 2D, 3D and 6D may carry novel alleles with potential to enhance grain weight due to the use of untapped wild accessions of Aegilops tauschii. Statistical simulations showed that favorable alleles for thousand kernel weight (TKW), grain length, width and thickness have additive genetic effects. Allelic variations for known genes controlling grain size and weight, viz. TaCwi-2A, TaSus-2B, TaCKX6-3D and TaGw2-6A, were also associated with TKW, grain width and thickness. In silico functional analysis predicted a range of biological functions for 32 DArT loci and receptor like kinase, known to affect plant development, appeared to be common protein family encoded by several loci responsible for grain size and shape. CONCLUSION: Conclusively, we demonstrated the application and integration of multiple approaches including high throughput phenotyping using DI, genome wide association studies (GWAS) and in silico functional analysis of candidate loci to analyze target traits, and identify candidate genomic regions underlying these traits. These approaches provided great opportunity to understand the breeding value of SHWs for improving grain weight and enhanced our deep understanding on molecular genetics of grain weight in wheat.

Project description:We used genotyping-by-sequencing (GBS) to investigate the evolutionary history of domesticated tetraploid wheats. With a panel of 189 wild and domesticated wheats, we identified 1,172,469 single nucleotide polymorphisms (SNPs) with a read depth ≥3. Principal component analyses (PCAs) separated the Triticum turgidum and Triticum timopheevii accessions, as well as wild T. turgidum from the domesticated emmers and the naked wheats, showing that SNP typing by GBS is capable of providing robust information on the genetic relationships between wheat species and subspecies. The PCAs and a neighbour-joining analysis suggested that domesticated tetraploid wheats have closest affinity with wild emmers from the northern Fertile Crescent, consistent with the results of previous genetic studies on the origins of domesticated wheat. However, a more detailed examination of admixture and allele sharing between domesticates and different wild populations, along with genome-wide association studies (GWAS), showed that the domesticated tetraploid wheats have also received a substantial genetic input from wild emmers from the southern Levant. Taking account of archaeological evidence that tetraploid wheats were first cultivated in the southern Levant, we suggest that a pre-domesticated crop spread from this region to southeast Turkey and became mixed with a wild emmer population from the northern Fertile Crescent. Fixation of the domestication traits in this mixed population would account for the allele sharing and GWAS results that we report. We also propose that feralization of the component of the pre-domesticated population that did not acquire domestication traits has resulted in the modern wild population from southeast Turkey displaying features of both the domesticates and wild emmer from the southern Levant, and hence appearing to be the sole progenitor of domesticated tetraploids when the phylogenetic relationships are studied by methods that assume a treelike pattern of evolution.

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Asymmetric gene expression in grain development of reciprocal crosses between tetraploid and hexaploid wheats.

Publications

Asymmetric gene expression in grain development of reciprocal crosses between tetraploid and hexaploid wheats.

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