Regulation of rose petal dehydration tolerance and senescence by RhNAP transcription factor via the modulation of cytokinin catabolism

Jing Zou,Liwei Jiang,Peitao Lü,Changqing Zhang,Jin Chen,Yusen Cui,Tao Zhang,Junping Gao,Yi Yao,Kun Liu

doi:10.1186/s43897-021-00016-7

Jing Zou, Liwei Jiang + Show 8 more

Open Access

https://doi.org/10.1186/s43897-021-00016-7

Copy DOI

Abstract

Petals and leaves share common evolutionary origins but have different phenotypic characteristics, such as the absence of stomata in the petals of most angiosperm species. Plant NAC transcription factor, NAP, is involved in ABA responses and regulates senescence-associated genes, and especially those that affect stomatal movement. However, the regulatory mechanisms and significance of NAP action in senescing astomatous petals is unclear. A major limiting factor is failure of flower opening and accelerated senescence. Our goal is to understand the finely regulatory mechanism of dehydration tolerance and aging in rose flowers. We functionally characterized RhNAP, an AtNAP-like transcription factor gene that is induced by dehydration and aging in astomatous rose petals. Cytokinins (CKs) are known to delay petal senescence and we found that a cytokinin oxidase/dehydrogenase gene 6 (RhCKX6) shares similar expression patterns with RhNAP. Silencing of RhNAP or RhCKX6 expression in rose petals by virus induced gene silencing markedly reduced petal dehydration tolerance and delayed petal senescence. Endogenous CK levels in RhNAP- or RhCKX6-silenced petals were significantly higher than those of the control. Moreover, RhCKX6 expression was reduced in RhNAP-silenced petals. This suggests that the expression of RhCKX6 is regulated by RhNAP. Yeast one-hybrid experiments and electrophoresis mobility shift assays showed that RhNAP binds to the RhCKX6 promoter in heterologous in vivo system and in vitro, respectively. Furthermore, the expression of putative signal transduction and downstream genes of ABA-signaling pathways were also reduced due to the repression of PP2C homolog genes by RhNAP in rose petals. Taken together, our study indicates that the RhNAP/RhCKX6 interaction represents a regulatory step enhancing dehydration tolerance in young rose petals and accelerating senescence in mature petals in a stomata-independent manner.

Highlights

Plant organ senescence is a finely tuned developmental process during which the constituent cells undergo dramatic changes in metabolism, structure and gene expression (Woo et al 2018; Ma et al 2018) and, programmed cell death (PCD)
Together with abscisic acid (ABA) signaling cascade mediated by RhNAP-RhPP2C interactions, we propose that RhNAPRhCKX6 associations regulate petal dehydration tolerance and senescence in rose flowers
RhNAP and RhCKX6 are co-expressed in response to dehydration and during petal senescence Based on our previous microarray results (Dai et al 2012), we identified a dehydration-induced unigene, JK619941, encoding a rose NAC family transcription factors (TFs)

Summary

Introduction

Plant organ senescence is a finely tuned developmental process during which the constituent cells undergo dramatic changes in metabolism, structure and gene expression (Woo et al 2018; Ma et al 2018) and, programmed cell death (PCD) (van Doorn and Woltering 2008; Kabbage et al 2017). It has been reported that senescence programs in both leaves and flowers involve the preferential expression of a specific set of senescence associated genes (SAGs), which include regulatory transcription factors (TFs) and structural proteins (Gao et al 2016; Li et al 2018; Sun et al 2021). Different classes of TF genes have been functionally associated with leaf and/or flower senescence, including MYB, MYC, C2H2-type zincfinger, AP2/EREBP, MADS-Box, NAC and WRKY domain TFs, as well as homeodomain proteins (Li et al 2018; Shahri and Tahir 2014). AtNAP is known to act together with a protein phosphatase 2C (PP2C) to mediate the abscisic acid (ABA) regulated promotion of stomatal opening and water loss in senescing leaves, as part of the ABAAtNAP-SAG113 PP2C signal transduction pathway (Zhang and Gan 2012). AtNAP homologs have been identified in rice (O. sativa) (Liang et al 2014) and morning glory (I. nil) (Shinozaki et al 2014)

Objectives

Results

Conclusion