Comparative tissue-specific transcriptomics reveals the regulatory control of convergent seed shattering in independently evolved weedy rice lineages

Abstract

The repeated evolution of high seed shattering during multiple independent de-domestications of cultivated Asian rice (Oryza sativa) into weedy rice (Oryza spp.) is a prime example of convergent evolution. Weedy rice populations converge in histological features of the abscission zone (AZ), a crucial structure for seed abscission, while ancestral cultivated rice populations exhibit varied AZ morphology and levels of shattering. However, the genetic bases of these phenotypic patterns remain unclear. We examined the expression profiles of the AZ region and its surrounding tissues at three developmental stages in two low-shattering cultivars of aus and temperate japonica domesticated groups and in two genotypes of their derived high-shattering weed groups, Blackhull Awned (BHA) and Spanish Weedy Rice (SWR), respectively. Consistent with the greater alteration of AZ morphology during the de-domestication of SWR than BHA, fewer genes exhibited a comparable AZ-region exclusive expression pattern between weed and crop in the temperate japonica lineage than in the aus lineage. Transcription factors related to the repression of lignin and secondary cell wall deposition, such as, OsWRKY102 and OsXND-1-like, along with certain known shattering genes involved in AZ formation, likely played a role in maintaining AZ region identity in both lineages. Meanwhile, most genes exhibiting AZ-region exclusive expression patterns do not overlap between the two lineages and the genes exhibiting differential expression in the AZ region between weed and crop across the two lineages are enriched for different gene ontology terms. Our findings suggest genetic flexibility in shaping AZ morphology, while genetic constraints on AZ identity determination in these two lineages.