Into the wild: quest for the novel regulatory mechanism, phenotypes, and genes in Oryza rufipogon, progenitor of cultivated rice

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2023-05

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Abstract

Rice is a crucial staple crop, but domestication for specific traits has resulted in decreased genetic diversity, leaving cultivated varieties vulnerable to various biotic and abiotic stresses. To develop the next generation of climate-ready cultivars, breeding programs need to focus on crop wild relatives that are rich in genetic diversity. The inter-species variation across the genus Oryza provides an opportunity to uncover novel gene functions and adaptive genetic mechanisms created by natural evolution. The study aims to explore the genome of Oryza rufipogon, the immediate progenitor of domesticated rice, and identify novel regulatory mechanisms, phenotypes, and genes. Our study hypothesized that the genome of wild O. rufipogon encodes novel mechanisms that allow survival and adaptation to sub-optimal environments. We describe the genomic uniqueness and divergence O. rufipogon relative to other known sources of salinity tolerance in the cultivated germplasm in context of its hidden potential to create transgressive traits for salinity tolerance. We compared the transcriptomic responses of four rice accessions representing a spectrum of variation for salinity response and investigated the divergence and conservation of transcriptomic fluxes of orthologous gene sets, spanning the domestication divide and salinity tolerance spectrum. We found that O. rufipogon is a novel source of salinity tolerance, and its fitness under salinity was associated with photosynthetic processes and hormonal activities, while in Pokkali, a well-known salinity tolerance line, ion homeostasis was the primary determinant of salt tolerance. In the next phase, we explored the cryptic genetic variation present in the genome of O. rufipogon in the creation of novel salinity tolerance phenotypes using a library of Chromosome Segment Substitution Lines (CSSLs). We identified novel salinity tolerant and susceptible lines beyond the parental ranges and also identified putative candidate expression quantitative trait loci (eQTLs) and cryptic genes that regulate the novel salinity-tolerant phenotypes by integrating comprehensive phenotyping, genomics, and transcriptomics. We also explored the genome of O. rufipogon for the BTB (Broad-complex, Tramtrack and Bric a brac) class of proteins, also known as POZ (Pox virus and Zinc finger) proteins, which are molecular ‘fine-tuners’ that integrate the various aspects of cellular adaptive responses. The aim was to determine their conservation, novelty, and potential applications for allele mining. We identified eight novel BTB/POZ genes in Oryza rufipogon genome with orthologs in its distant cousins in the family Poaceae (Sorghum, Brachypodium), but these orthologs appear to have been lost in the domesticated descendant, O. sativa ssp. japonica. Comparative sequence analysis and structure comparisons of these novel OrBTB genes showed that diverged upstream regulatory sequences and regulon restructuring are key features of the evolution of this large gene family. Overall, this study reveals the untapped potential of genetic novelties in crop wild relatives that can enhance the genetic diversity, helps in tailoring climate resilience of rice cultivars, and lays the groundwork for functional genomic studies to identify and transfer genes from the wild rice gene pool into rice breeding programs.


Embargo status: Restricted until 06/2025. To request the author grant access, click on the PDF link to the left.

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Keywords

Rice,, Crop wild relatives,, Salinity,, Oryza rufipogon,, Broad-complex, Tramtrack and Bric a brac (BTB)

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