CRISPR‐based assessment of genomic structure in the conserved SQUAMOSA promoter‐binding‐like gene clusters in rice. (30th October 2020)

• Record Type: Journal Article
• Authors: Jiang, Mengmeng; He, Ying; Chen, Xiaonan; Zhang, Xiaohui; Guo, Yanru; Yang, Sihai; Huang, Ju; Traw, M. Brian
• Is Part Of: Plant journal. Volume 104:Number 5(2020)
• Page Start: 1301
• Page End: 1314
• Publication Date: 2020-10-30
• Subjects: SPL family -- whole genome duplication -- genomic architecture -- expression network -- subfunctionalization -- Oryza sativa.; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.15001
• Languages: English
• ISSNs: 0960-7412

Abstract

SUMMARY: Although SQUAMOSA promoter‐binding‐like (SPL) transcription factors are important regulators of development in rice ( Oryza sativa ), prior assessments of the SPL family have been limited to single genes. A functional comparison across the full gene family in standardized genetic backgrounds has not been reported previously. Here, we demonstrate that the SPL gene family in rice is enriched due to the most recent whole genome duplication (WGD). Notably, 10 of 19 rice SPL genes (52%) cluster in four units that have persisted for at least 50 million years. We show that SPL gene grouping and retention following WGD is widespread in angiosperms, suggesting the conservatism and importance of this gene arrangement. We used Cas9 editing to generate transformation lines for all 19 SPL genes in a common set of backgrounds, and found that knockouts of 14 SPL genes exhibited defects in plant height, 10 exhibited defects in panicle size, and nine had altered grain lengths. We observed subfunctionalization of genes in the paleoduplicated pairs, but little evidence of neofunctionalization. Expression of OsSPL3 was negatively correlated with that of its closest neighbor in its synteny group, OsSPL4, and its sister paired gene, OsSPL12, in the opposing group. Nucleotide diversity was lower in eight of the nine singleton genes in domesticated rice, relative to wild rice, whereas the reverse was true for the paired genes. Together, these results provide functional information on eight previously unexamined OsSPL family members and suggest that paleoduplicate pair redundancy benefits plant survival and innovation. Abstract : We show here conserved paired unit clustering of SPL transcription factors in rice, and document that the pattern is widespread in monocots and dicots. Through comprehensive Cas9 editing of the 19‐member OsSPL family, we find subfunctionalization but not neofunctionalization between paired genes, and widespread fitness‐related defects. We report expression interactions both within and between gene groups. These findings are important to our understanding of gene functional redundancy and retention across evolutionary time.