H2O2 as a Feedback Signal on Dual-Located WHIRLY1 Associates with Leaf Senescence in Arabidopsis

Abstract

Leaf senescence, either as a natural stage of development or as an induced process under stress conditions, incorporates multiple intricate signaling pathways. At the cellular level, retrograde signals have been considered as important players during the initiation and progression of senescence in both animals and plants. The plant-specific single-strand DNA-binding protein WHIRLY1 (WHY1), a repressor of leaf natural senescence, is dually located in both nucleus and plastids. Despite many years of studies, the myth about its dual location and the underlying functional implications remain elusive. Here, we provide further evidence in Arabidopsis showing that alteration in WHY1 allocation between the nucleus and chloroplast causes perturbation in H2O2 homeostasis, resulting in adverse plant senescence phenotypes. The knockout of WHY1 increased H2O2 content at 37 days post-germination, coincident with an early leaf senescence phenotype, which can be rescued by ectopic expression of the nuclear isoform (nWHY1), but not by the plastid isoform (pWHY1). Instead, accumulated pWHY1 greatly provoked H2O2 in cells. On the other hand, exogenous H2O2 treatment induced a substantial plastid accumulation of WHY1 proteins and at the same time reduced the nuclear isoforms. This H2O2-induced loss of nucleus WHY1 isoform was accompanied by enhanced enrichments of histone H3 lysine 9 acetylation (H3K9ac) and recruitment of RNA polymerase II (RNAP II) globally, and specifically at the promoter of the senescence-related transcription factor WRKY53, which in turn activated WRKY53 transcription and led to a senescence phenotype. Thus, the distribution of WHY1 organelle isoforms and the feedback of H2O2 intervene in a circularly integrated regulatory network during plant senescence in Arabidopsis.

Translocation of chloroplast NPR1 to the nucleus in retrograde signaling for adaptive response to salt stress in tobacco

“…For example, WHIRLY1, which belongs to a small plant-specific family of DNA/RNA binding proteins, has been proposed to move from the chloroplast to the nucleus in response to environmental cues, such as high light intensity (Foyer et al, 2014; Świda-Barteczka et al, 2018). However, it did not seem to be translocated from chloroplasts to the nucleus, but rather it was more likely that the WHIRLY1 protein comprised two isoforms localized in the chloroplasts and the nucleus, respectively (Lin et al, 2019). The dual functions of WHIRLY1 may be associated with its dual localization for coordination of the retrograde signaling from plastids to the nucleus (Ren et al, 2017).…”

A new factor in the circadian control of barley chloroplast development

“…It also has chaperone functions in RNA processing in chloroplasts (Pfalz et al, 2006;Prikryl et al, 2008;Meloneck et al, 2010;Świda-Barteczka et al, 2018). WHY1 is also associated with the thylakoid membrane and has putative functions in photosynthesis (Isemer et al, 2012;Foyer et al, 2014;Comadira et al, 2015;Huang et al, 2017;Guan et al, 2018;Lin et al, 2019). An earlier study on knockdown maize ZmWhy1 mutants, which have a pale green phenotype (Prikryl et al, 2008) suggested that WHY1 is involved in chloroplast biogenesis.…”

Here, There, and Everywhere: Plastid- and Nuclear-Localized WHIRLY1 Regulates Salicylic Acid Homeostasis during Developmental Senescence

“…All three WHY proteins bind single-stranded DNA, and perhaps RNA, in a sequence-nonspecific manner (Desveaux et al, 2002;Bach-Pages et al, 2020). WHY1 is partitioned between the nucleus and chloroplast (Krause et al, 2005;Grabowski et al, 2008); however, the mechanisms that might determine its distribution in the cell are only starting to emerge (Ren et al, 2017;Lin et al, 2019). In the nucleus, WHY1 controls the expression of transcription factors, defense genes, and senescence genes by binding their promoters (Krupinska et al, 2013;Ren et al, 2017).…”

“…To establish which of the two WHY1 isoforms affects SA metabolism, the authors complemented why1 with plastid, nuclear, or the full-length WHY1 isoforms (Lin et al, 2019). Full-length WHY1 has both a plastid-target peptide for plastid import and a nuclear localization signal.…”

“…Several factors have been shown to affect the organellar distribution of WHY1 including cellular redox state (H 2 O 2 signals) and the WHY1 phosphorylation state (Ren et al, 2017;Lin et al, 2019). In this study, Lin et al (2020) added SA to the list (Fig.…”