Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis

Abstract

Plants initiate senescence to shed photosynthetically inefficient leaves. Light deprivation induces leaf senescence, which involves massive transcriptional reprogramming to dismantle cellular components and remobilize nutrients. In darkness, intermittent pulses of red light can inhibit senescence, likely via phytochromes. However, the precise molecular mechanisms transducing the signals from light perception to the inhibition of senescence remain elusive. Here, we show that in Arabidopsis, dark-induced senescence requires phytochrome-interacting transcription factors PIF4 and PIF5 (PIF4/PIF5). ELF3 and phytochrome B inhibit senescence by repressing PIF4/PIF5 at the transcriptional and post-translational levels, respectively. PIF4/PIF5 act in the signalling pathways of two senescence-promoting hormones, ethylene and abscisic acid, by directly activating expression of EIN3, ABI5 and EEL. In turn, PIF4, PIF5, EIN3, ABI5 and EEL directly activate the expression of the major senescence-promoting NAC transcription factor ORESARA1, thus forming multiple, coherent feed-forward loops. Our results reveal how classical light signalling connects to senescence in Arabidopsis.

ABA receptor PYL9 promotes drought resistance and leaf senescence

“…When phosphorylated by SnRK2s, RAV1 and ABFs increase the expression of NAC transcription factors through ABRE motifs and/or RAV1-binding motifs ( Fig. S8C) (8). These NAC transcription factors promote the expression of downstream SAGs, which in turn, control leaf senescence (5)(6)(7)34).…”

“…Environmental stimuli and phytohormones may regulate leaf senescence through NACs. Phytochrome-interacting factor 4 (PIF4) and PIF5 transcription factors promote dark-induced senescence by activating ORE1 expression (8). The expression of ORE1, AtNAP, and OsNAP (ortholog of AtNAP) is up-regulated by ABA by an unknown molecular mechanism (7,9).…”

Phytochromes and Phytochrome Interacting Factors

“…2; Hornitschek et al, 2009;Hao et al, 2012;Lee et al, 2014;Nieto et al, 2015). Besides hypocotyl elongation, PIF4 also controls several physiological and development aspects, such as stomatal development in response to light quality, circadian gating, chlorophyll degradation and leaf senescence in darkness, freezing tolerance, and anthocyanin biosynthesis under red-light conditions Casson et al, 2009;Lee and Thomashow, 2012;Sakuraba et al, 2014;Song et al, 2014;Liu et al, 2015;Zhang et al, 2015;Zhu et al, 2016a).…”

“…PIF5 (and PIF4) functions as a positive regulator of leaf senescence through chlorophyll degradation in darkness (Sakuraba et al, 2014;Song et al, 2014;Zhang et al, 2015) and as a negative regulator of red light-induced anthocyanin biosynthesis . PIF5 in collaboration with PIF4 and PIF7 functions as an important regulator of shade avoidance in Arabidopsis Hornitschek et al, 2009;Li et al, 2012a).…”

A Negative Feedback Loop between PHYTOCHROME INTERACTING FACTORs and HECATE Proteins Fine-Tunes Photomorphogenesis in Arabidopsis

“…A quadruple pif1 pif3 pif4 pif5 mutant displayed constitutive photomorphogenic phenotypes both morphologically and at the gene expression level in the dark (Leivar et al, 2008(Leivar et al, , 2009Shin et al, 2009), suggesting that PIFs repress photomorphogenic growth in the dark. In addition to photomorphogenesis, PIFs regulate many other pathways, including circadian clock, flowering time in response to temperature, stomatal development, and senescence, suggesting that PIFs act as signaling hubs in regulating plant growth and development (Leivar and Monte, 2014;Sakuraba et al, 2014).…”