Integrative transcriptome and metabolome analyses to uncover rice panicle branch albinism

Abstract

Chloroplast development is essential for photosynthesis and overall plant viability. While leaf and whole panicle albinism has been extensively studied as a model for chloroplast biogenesis, the genetic mechanisms underlying tissue-specific chloroplast development in reproductive organs, such as panicle branches, remain poorly understood, specifically how these tissues manage photoprotection under various panicle developmental constraints. Here, we characterized a rice white panicle branch natural mutant “ wpb1” , which impairs chloroplast biogenesis, leading to albino panicles and seedling segregation in hybrid progenies. Phenotypic analysis showed limited pro-plastid proliferates during stages III-IV and a complete failure in thylakoid formation during stages VI-VII in the wpb1 mutant as compared to wild type. Integrated transcriptomic and metabolomic profiling uncovered the molecular cascade associated with phenotype; at the onset of phenotypic divergence, a significant downregulation of carotenoid biosynthesis genes, including those for lutein, coincided with the loss of photoprotection. This deficiency was accompanied by oxidative damage to photosynthetic apparatus, sustained upregulation of reactive oxygen species and heat shock responses. Our data suggests a model in which failure to quench singlet oxygen and excited chlorophyll molecules via xanthophyll cycle ultimately blocks greening, leading to oxidative damage and the inability of tissue to turn green. Changes in many core metabolic pathways, such as those for alanine and isoprenoids, suggests a substantial rewiring of core metabolism. Collectively, our findings identify a key node where wpb1 disrupts the coordination between photoprotective pigment accumulation and chloroplast development, providing new insights into the genetic regulation photosynthesis in rice panicle branches.