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Study Reveals Rice Genes Involved in Hybrid Sterility

NEW YORK (GenomeWeb News) – Fertility-fighting versions of three genes at the same genetic locus contribute to hybrid sterility in plants produced by crossing two popular rice sub-species, according to a study appearing online today in Science.

Researchers from Huazhong Agricultural University and Chinese University of Hong Kong used gene sequencing, genotyping, and other strategies to delve into the genetics of hybrid sterility in the offspring of rice (Oryza sativa) crosses between japonica and indica sub-species. Their analyses suggest that a trio of genes within a shared locus in the rice genome participate in an antagonistic "killer-protective" system that impacts spore formation in female plants and influences gene segregation ratios.

Because hybrid sterility "is a major form of post-zygotic reproductive isolation that restricts gene flow between populations," explained senior author Qifa Zhang, a researcher with Huazhong Agricultural University's National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research, and co-authors, the latest insights into this process "add to our understanding of differences between indica and japonica rice and may aid in rice genetic improvement."

The researchers focused their attention on a section of the rice genome known as S5, one of several loci implicated in rice hybrid sterility in past studies of indica-japonica hybrid plants. The locus varies between these two sub-species, they explained, and generally contains as many as five open reading frames.

To better understand sub-species-specific patterns at the S5 locus and their effects on fertility, the team sequenced and compared genes in this region in plants from rice varieties: the indica sub-species variety known as Nanjing 11, a japonica variety called Balilla, and two varieties — called Dular and 02428 — that produce fertile offspring with both of sub-species.

Based on their sequence comparisons, coupled with follow-up experiments, researchers identified three open reading frames — dubbed ORF3, ORF4, and ORF5 — that not only contribute to sterility in indica-japonica hybrids, but also influence fertility features in the parental sub-species.

In particular, the study authors explained, these three genes appear to code for components of a so-called "killer-protector system." The ORF4 gene product helps a protein produced from the ORF5 "killer" gene exert stress on the membranous endoplasmic reticulum network within the female rice cells tasked with producing spores.

Meanwhile, an opposing "protector" gene, ORF3, codes for a protein that prevents this stress, defending developing gametes against premature death.

Within japonica varieties, the protective function of ORF3 is lacking due to a frameshift deletion that renders its protein product powerless against the stress-inducing killer gene.

In that genetic background, the killer gene ORF5 is not as potent, allowing the plants to reproduce. But when the japonica plants are crossed with indica plants, which generally have ORF3+, ORF5+, and ORF4- profiles, gene segregation in the S5 locus is such that the offspring often carry a muted ORF3 protector gene in the presence of fully functional killer genes. And that, say researchers, causes premature cell death at the embryo-sac stage of seed formation.

"This killer-protective system may have a profound implication in the evolution and diversification of rice," the study authors noted.

"Reproductive isolation enforced by the killer (ORF4+, ORF5+) would have promoted genetic differentiation between indica and japonica rice, which appears to be a major source of genetic diversity in the rice gene pool," they explained, "whereas the protector (ORF3+) and non-killer combinations of ORF4 and ORF5 would allow for hybridization and gene flow, thus providing a coherent force at the species level."

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