Chromosome-scale genome assembly provides insights into rye biology, evolution and agronomic potential

Rabanus‐Wallace, M. Timothy; Hackauf, Bernd; Mascher, Martin; Lux, Thomas; Wicker, Thomas; Gundlach, Heidrun; Báez, Mariana; Houben, Andreas; Mayer, Klaus; Guo, Liangliang; Poland, Jesse; Pozniak, Curtis; Walkowiak, Sean; Melonek, Joanna; Praz, Coraline R.; Schreiber, Mona; Budak, Hikmet; Heuberger, Matthias; Steuernagel, Burkhard; Wulff, Brande B. H.; Börner, Andreas; Byrns, Brook; Čížková, Jana; Fowler, D. B.; Fritz, Allan K.; Himmelbach, Axel; Kaithakottil, Gemy; Keilwagen, Jens; Keller, Beat; Konkin, David; Larsen, Julie S.; Li, Qiang; Myśków, Beata; Padmarasu, Sudharsan; Rawat, Nidhi; Sesiz, Uğur; Biyiklioglu-Kaya, Sezgi; Sharpe, Andy; Šimková, Hana; Small, Ian; Swarbreck, David; Toegelová, Helena; Tsvetkova, Natalia; Voylokov, A. V.; Vrána, Jan; Bauer, Eva; Bolibok-Brągoszewska, Hanna; Doležel, Jaroslav; Hall, Anthony; Jia, Jizeng; Korzun, Viktor; Laroche, André; Xue, Feng; Ordon, Frank; Özkan, Hakan; Rakoczy-Trojanowska, Monika; Scholz, Uwe; Schulman, Alan H.; Siekmann, Dörthe; Stojałowski, Stefan; Tiwari, Vijay K.; Spannagl, Manuel; Stein, Nils

doi:10.1038/s41588-021-00807-0

Cited by 178 publications

(197 citation statements)

References 77 publications

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“…However, on a phenotypic level, the perenniality in our study differed from the other crops, because there, perennial genotypes were simultaneously characterized by rhizomatous growth. On a genomic level, it was difficult to make proper comparisons, because so far for rye only reference genome sequences for the annual crop (S. cereale) had been published [47,48] and functional perennation genes could principally only be found in genomes of perennial species (genotypes). If we expect similar genes for perenniality across cereals, the comparison of genomic sequences from perennation-associated QTLs in perennial species could be a valuable resource to dissect perennation from related traits and to filter the vast amount of potential gene candidates.…”

Section: Species Syntenymentioning

confidence: 99%

Perennial Rye: Genetics of Perenniality and Limited Fertility

Gruner

Miedaner

2021

Plants

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Perenniality, the ability of plants to regrow after seed set, could be introgressed into cultivated rye by crossing with the wild relative and perennial Secale strictum. However, studies in the past showed that Secale cereale × Secale strictum-derived cultivars were also characterized by reduced fertility what was related to so called chromosomal multivalents, bulks of chromosomes that paired together in metaphase I of pollen mother cells instead of only two chromosomes (bivalents). Those multivalents could be caused by ancient translocations that occurred between both species. Genetic studies on perennial rye are quite old and especially the advent of molecular markers and genome sequencing paved the way for new insights and more comprehensive studies. After a brief review of the past research, we used a basic QTL mapping approach to analyze the genetic status of perennial rye. We could show that for the trait perennation 0.74 of the genetic variance in our population was explained by additively inherited QTLs on chromosome 2R, 3R, 4R, 5R and 7R. Fertility on the other hand was with 0.64 of explained genetic variance mainly attributed to a locus on chromosome 5R, what was most probably the self-incompatibility locus S5. Additionally, we could trace the Z locus on chromosome 2R by high segregation distortion of markers. Indications for chromosomal co-segregation, like multivalents, could not be found. This study opens new possibilities to use perennial rye as genetic resource and for alternative breeding methods, as well as a valuable resource for comparative studies of perennation across different species.

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Section: Species Syntenymentioning

confidence: 99%

Perennial Rye: Genetics of Perenniality and Limited Fertility

Gruner

Miedaner

2021

Plants

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“…The availability of the sequenced rye genome (https://www.ncbi.nlm.nih.gov/assembly/ GCA_902687465.1, accessed on 9 December 2020) made it possible to describe the structure of the CENH3 locus and to compare the structure of this locus in closely related species, barley and wheat. The size of the CENH3 locus in rye line Lo7 [17] from the left-border (upstream) gene, LHCB3-l (LHCB3-like), which contains the domain of chlorophyll a-b binding protein 3C, to the right-border (downstream) gene, bZIP, which is a transcription factor gene, is 218.3 kb (Figure 1).…”

Section: Molecular Organization Of the Cenh3 Locus In Ryementioning

confidence: 99%

“…However, the structure of the entire CENH3 locus, the expression levels of the genes encoding the CENH3 proteins and the efficiency of these proteins loading into chromosomes remain unknown. The sequencing of two rye accessions [17,18] makes it possible to thoroughly explore the coding and regulatory parts of the αCENH3 and βCENH3 genes. In addition, it becomes possible to address how their features correlate with the expression levels of these genes and the localization of the proteins in chromosomes and nuclei at different stages of plant development.In this work, we investigated the organization of the CENH3 locus in the S. cereale genome to identify functionally important sites in the vicinity of the αCENH3 and βCENH3 genes.…”

Section: Introductionmentioning

confidence: 99%

Expression of Two Rye CENH3 Variants and Their Loading into Centromeres

Евтушенко

Elisafenko

Gatzkaya

et al. 2021

Plants

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Gene duplication and the preservation of both copies during evolution is an intriguing evolutionary phenomenon. Their preservation is related to the function they perform. The central component of centromere specification and function is the centromere-specific histone H3 (CENH3). Some cereal species (maize, rice) have one copy of the gene encoding this protein, while some (wheat, barley, rye) have two. Therefore, they represent a good model for a comparative study of the functional activity of the duplicated CENH3 genes and their protein products. We determined the organization of the CENH3 locus in rye (Secale cereale L.) and identified the functional motifs in the vicinity of the CENH3 genes. We compared the expression of these genes at different stages of plant development and the loading of their products, the CENH3 proteins, into nucleosomes during mitosis and meiosis. Using extended chromatin fibers, we revealed patterns of loading CENH3proteinsinto polynucleosomal domains in centromeric chromatin. Our results indicate no sign of neofunctionalization, subfunctionalization or specialization in the gene copies. The influence of negative selection on the coding part of the genes led them to preserve their conserved function. The advantage of having two functional genes appears as the gene-dosage effect.

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“…While the P class has predominantly been associated with RFL-PPR genes, instances of the PLS class have also been identified [35]. In rye, 591 PPR genes have been identified, out of which 83 belong to the RFL-PPR clade [36] (Table S8a). PPR proteins target mitochondrial or chloroplast mRNA, participating in a range of post-transcriptional processes (RNA editing, splicing, cleavage, and translation) with profound effects on organelle biogenesis and function [33,37,38].…”

Section: Introductionmentioning

confidence: 99%

“…Within grasses, several isolated Rf genes have been characterized as RFL-PPRs, including Rfm1 in barley [35], Rf1 in sorghum (Sorghum bicolore L.) [40], Rf5 in maize [41], and Rf4, Rf5, and Rf6 in rice (Oryza sativa L.) [42][43][44]. In the C-type CMS system of rye, the Rfc1 locus has been found to reside in close proximity to a cluster of RFL-PPR genes on 4RL [36].…”

Section: Introductionmentioning

confidence: 99%

Genomic Scan of Male Fertility Restoration Genes in a ‘Gülzow’ Type Hybrid Breeding System of Rye (Secale cereale L.)

Vendelbo

Mahmood²,

Sarup³

et al. 2021

IJMS

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Efficient and stable restoration of male fertility (Rf) is a prerequisite for large-scale hybrid seed production but remains an inherent issue in the predominant fertility control system of rye (Secale cereale L.). The ‘Gülzow’ (G)-type cytoplasmic male sterility (CMS) system in hybrid rye breeding exhibits a superior Rf. While having received little scientific attention, one major G-type Rf gene has been identified on 4RL (Rfg1) and two minor genes on 3R (Rfg2) and 6R (Rfg3) chromosomes. Here, we report a comprehensive investigation of the genetics underlying restoration of male fertility in a large G-type CMS breeding system using recent advents in rye genomic resources. This includes: (I) genome-wide association studies (GWAS) on G-type germplasm; (II) GWAS on a biparental mapping population; and (III) an RNA sequence study to investigate the expression of genes residing in Rf-associated regions in G-type rye hybrids. Our findings provide compelling evidence of a novel major G-type non-PPR Rf gene on the 3RL chromosome belonging to the mitochondrial transcription termination factor gene family. We provisionally denote the identified novel Rf gene on 3RL RfNOS1. The discovery made in this study is distinct from known P- and C-type systems in rye as well as recognized CMS systems in barley (Hordeum vulgare L.) and wheat (Triticum aestivum L.). We believe this study constitutes a stepping stone towards understanding the restoration of male fertility in the G-type CMS system and potential resources for addressing the inherent issues of the P-type system.

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Chromosome-scale genome assembly provides insights into rye biology, evolution and agronomic potential

Cited by 178 publications

References 77 publications

Perennial Rye: Genetics of Perenniality and Limited Fertility

Perennial Rye: Genetics of Perenniality and Limited Fertility

Expression of Two Rye CENH3 Variants and Their Loading into Centromeres

Genomic Scan of Male Fertility Restoration Genes in a ‘Gülzow’ Type Hybrid Breeding System of Rye (Secale cereale L.)

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