CCCH protein-PvCCCH69 acted as a repressor for leaf senescence through suppressing ABA-signaling pathway

Zheni Xie,Chenchen Zhang,Shanshan Lei,Guohui Yu,Bin Xu Bin Xu,Bingru Huang

doi:10.1038/s41438-021-00604-0

Abstract

CCCH is a subfamily of zinc finger proteins involved in plant growth, development, and stresses response. The function of CCCH in regulating leaf senescence, especially its roles in abscisic acid (ABA)-mediated leaf senescence is largely unknown. The objective of this study was to determine functions and mechanisms of CCCH gene in regulating leaf senescence in switchgrass (Panicum virgatum). A CCCH gene, PvCCCH69 (PvC3H69), was cloned from switchgrass. Overexpressing PvC3H69 in rice suppressed both natural senescence with leaf aging and dark-induced leaf senescence. Endogenous ABA content, ABA biosynthesis genes (NCED3, NCED5, and AAO3), and ABA signaling-related genes (SnRKs, ABI5, and ABF2/3/4) exhibited significantly lower levels in senescencing leaves of PvC3H69-OE plants than those in WT plants. PvC3H69-suppression of leaf senescence was associated with transcriptional upregulation of genes mainly involved in the light-dependent process of photosynthesis, including light-harvesting complex proteins, PSI proteins, and PSII proteins and downregulation of ABA biosynthesis and signaling genes and senescence-associated genes. PvC3H69 could act as a repressor for leaf senescence via upregulating photosynthetic proteins and repressing ABA synthesis and ABA signaling pathways.

Highlights

Natural or stress-induced leaf senescence adversely affects photosynthetic capacity and plant productivity[1,2,3]
The CCCH-type zinc finger family includes multiple genes, and PvC3H69 cloned from switchgrass in our study was found to be a homology of ZmC3H38 and OsTZF124, but exhibited unique characteristics from the homologs in maize and rice
CCCH genes are known to regulate leaf senescence, different genes in the CCCH family were found to have distinct functions with AtKHZ1 and AtKHZ2 being characterized as a positive regulator inducing leaf senescence in Arabidopsis[6] and OsDOS and OsTZF1 as a negative regulator of leaf senescence in rice[7,8,9]

Summary

Introduction

Natural or stress-induced leaf senescence adversely affects photosynthetic capacity and plant productivity[1,2,3]. Leaf senescence development is regulated at multiple levels, involving molecular, transcriptional, posttranscriptional, and metabolic processes[3,4,5]. CCCH zinc finger proteins with three Cys and one His residues as the conserved motif that function as RNA-binding proteins and regulate RNA metabolism have been found to act as key regulators of leaf senescence in Arabidopsis thaliana and rice CCCH genes, AtKHZ1 and AtKHZ2, can accelerate leaf senescence when overexpressed in Arabidopsis[6]. OsDOS and OsTZF1 were found to be negative regulators of leaf senescence in rice[7,8,9]. Despite the knowledge of the involvement of CCCH genes in leaf senescence, the upstream and downstream regulatory mechanisms of CCCHs controlling leaf senescence remain largely unknown

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