Pheophorbide a, a chlorophyll catabolite may regulate jasmonate signalling during dark-induced senescence in Arabidopsis

Abstract

Chlorophyll degradation is one of the most visible landmarks of leaf senescence. During senescence, chlorophyll is degraded in the multi-step pheophorbide a oxygenase (PAO)/phyllobilin pathway, which is tightly regulated at the transcriptional level. This regulation allows a coordinated and efficient remobilisation of nitrogen towards sink organs. Taking advantage of combined transcriptome and metabolite analyses during dark-induced senescence of Arabidopsis thaliana mutants deficient in key steps of the PAO/phyllobilin pathway, we show an unanticipated role for one of the pathway intermediates, i.e. pheophorbide a. Both jasmonic acid-related gene expression and jasmonic acid precursors specifically accumulated in pao1, deficient in PAO. We propose that pheophorbide a, the last intact porphyrin intermediate of chlorophyll degradation and unique pathway ‘bottleneck’, has been recruited as a signalling molecule of the chloroplast metabolic status. Our work challenges the assumption that chlorophyll breakdown is merely a senescence output, but propose that the flux of pheophorbide a through the pathway acts in a feed-forward loop that remodels the nuclear transcriptome and controls the pace of chlorophyll degradation in senescing leaves.SummaryTranscriptome and metabolite profiles of key chlorophyll breakdown mutants reveal complex interplay between speed of chlorophyll degradation and jasmonic acid signallingFinancial sourcesThis work was supported by the European Union (Plant Fellow program), the Swiss National Foundation/ERA-NET (grant N° 163504) and the German Research Foundation (DFG, grant N° INST 186/822-1).

Chlorophyll breakdown—Regulation, biochemistry and phyllobilins as its products

“…The observed cell death was proposed to be due to highly photodynamic properties considered for both Pheide a and RCC (Mach, Castillo, Hoogstraten, & Greenberg, 2001;Pružinská et al, 2003;Tanaka, Hirashima, Satoh, & Tanaka, 2003). Interestingly, in addition to light-dependent lesion formation, pao/acd1, but not rccr/acd2 mutants also show light-independent cell death, when leaf senescence is induced in constant darkness (Aubry et al, 2018;Hirashima, Tanaka, & Tanaka, 2009). This led to the hypothesis (Kuai et al, 2018),…”

“…Since no further signaling molecules are known in this context, it still remains unclear how light-independent cell death is triggered. Interestingly, in Arabidopsis pao1 mutant plants, hundreds of genes are differentially expressed already in green tissues before the onset of senescence (Aubry et al, 2018), suggesting an important role of PAO apart from senescence-associated Chl breakdown.…”