Spatial Regulation of Rice Leaf Morphology by miRNA-Target Complexes During Viral Infection

Abstract

Leaf morphogenesis is essential for plant growth and development, yet the mechanisms by which plant viruses induce changes in leaf shape are not well understood. Rice ragged stunt virus (RRSV) infection induces distinct morphological abnormalities in rice leaves, including leaf tip curling and serrated margins, through unknown pathogenic mechanisms. This study reveals that key regulatory microRNAs (miR164, miR319 and miR156) and their target genes (CUC, TCP and SPL) exhibit entirely opposite expression patterns in healthy and RRSV-infected leaves, indicating a profound impact on the leaf morphogenesis network. Significantly, the core protein OsCUC1, which typically functions by forming dimers, shows abnormal expression in the peripheral zone of the shoot apical meristem under viral infection, leading to disruptions in leaf development. OsTCP1 was found to dynamically regulate OsCUC1 dimer formation by modifying its subcellular localization and interacting with OsSPL14 and OsSPL17, thereby influencing their regulatory functions. Genetic disruptions of OsCUC1, OsTCP1 and OsSPL14/OsSPL17 enhance the severity of RRSV infection, demonstrating their critical involvement in the viral pathogenic strategy. The research uncovers a novel mechanism by which RRSV manipulates the expression and interactions of key regulatory factors, disrupting the delicate balance of the leaf morphogenesis network. These findings expand our understanding of viral manipulation of host development and provide a foundation for innovative strategies to enhance crop resilience.