A coherent feedforward loop design principle to sustain robustness of biological networks

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.

show abstract

“…7). Such coherent feed-forward loops make a pathway less prone to being disturbed by ephemeral environmental fluctuations 48 .…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2014

View full text Add to dashboard Cite

show abstract

“…In other words, both PIF1 and the PIF1-dependent group A bZIPs regulate a subset of PIF1-dependent genes. Signaling pathways that include such coherent feed-forward loops are highly robust (Le and Kwon, 2013), and this is not the only such PIF1-dependent loop in imbibed seeds. PIF1 also activates the genes necessary for ABA biosynthesis, increasing the level of ABA in imbibed seeds (Oh et al, 2007(Oh et al, , 2009).…”

Section: Discussionmentioning

confidence: 99%

PIF1-Interacting Transcription Factors and Their Binding Sequence Elements Determine the in Vivo Targeting Sites of PIF1

et al. 2016

View full text Add to dashboard Cite

The bHLH transcription factor PHYTOCHROME INTERACTING FACTOR1 (PIF1) binds G-box elements in vitro and inhibits light-dependent germination in Arabidopsis thaliana. A previous genome-wide analysis of PIF1 targeting indicated that PIF1 binds 748 sites in imbibed seeds, only 59% of which possess G-box elements. This suggests the G-box is not the sole determinant of PIF1 targeting. The targeting of PIF1 to specific sites could be stabilized by PIF1-interacting transcription factors (PTFs) that bind other nearby sequence elements. Here, we report PIF1 targeting sites are enriched with not only G-boxes but also with other hexameric sequence elements we named G-box coupling elements (GCEs). One of these GCEs possesses an ACGT core and serves as a binding site for group A bZIP transcription factors, including ABSCISIC ACID INSENSITIVE5 (ABI5), which inhibits seed germination in abscisic acid signaling. PIF1 interacts with ABI5 and other group A bZIP transcription factors and together they target a subset of PIF1 binding sites in vivo. In vitro single-molecule fluorescence imaging confirms that ABI5 facilitates PIF1 binding to DNA fragments possessing multiple G-boxes or the GCE alone. Thus, we show in vivo PIF1 targeting to specific binding sites is determined by its interaction with PTFs and their binding to GCEs.

show abstract

“…S4), indicating that the NAC016-NAP-AAO3-ABA regulatory module forms a coherent feed-forward loop for activating leaf senescence, including Chl degradation. Similar feed-forward loops were found in the leaf senescence pathway of Arabidopsis (Kim et al 2009;Sakuraba et al 2014a), and may make the senescence pathway less prone to disruption by ephemeral environmental fluctuations (Le and Kwon, 2013).…”

Section: Discussionmentioning

confidence: 59%

Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription

et al. 2015

View full text Add to dashboard Cite

The Arabidopsis transcriptional factor NAC016 directly activates chlorophyll degradation during leaf senescence by binding to the promoter of SGR1 and upregulating its transcription. During leaf senescence or abiotic stress in Arabidopsis thaliana, STAYGREEN1 (SGR1) promotes chlorophyll (Chl) degradation, acting with Chl catabolic enzymes, but the mechanism regulating SGR1 transcription remains largely unknown. Here, we show that the Arabidopsis senescence-associated NAC transcription factor NAC016 directly activates SGR1 transcription. Under senescence-promoting conditions, the expression of SGR1 was downregulated in nac016-1 mutants and upregulated in NAC016-overexpressing (NAC016-OX) plants. By yeast one-hybrid and chromatin immunoprecipitation assays, we found that NAC016 directly binds to the SGR1 promoter, which contains the NAC016-specific binding motif (termed the NAC016BM). Furthermore, nac016-1 SGR1-OX plants showed an early leaf yellowing phenotype, similar to SGR1-OX plants, confirming that NAC016 directly activates SGR1 expression in the leaf senescence regulatory cascade. Although we found that NAC016 activates SGR1 expression in senescing leaves, this transcriptional regulation is considerably weaker in maturing seeds; the seeds of sgr1-1 mutants (also known as nonyellowing1-1, nye1-1) stayed green, while the seeds of nac016-1 mutants turned from green to yellow normally. We also found that the abscisic acid (ABA) signaling-related transcription factor genes ABI5 and EEL and the ABA biosynthesis gene AAO3, which activate SGR1 expression directly or indirectly, were significantly downregulated in nac016-1 mutants and upregulated in NAC016-OX plants. However, the NAC016BM does not exist in their promoter regions, indicating that NAC016 may indirectly activate these ABA signaling and biosynthesis genes, probably by directly activating transcriptional cascades regulated by the NAC transcription factor NAP. The NAC016-mediated regulatory cascades of SGR1 and other Chl degradation-related genes are discussed. and chromatin immunoprecipitation assays, we found that NAC016 directly binds to the SGR1 21 promoter, which contains the NAC016-specific binding motif (termed the NAC016BM). 22Furthermore, nac016-1 SGR1-OX plants showed an early leaf yellowing phenotype, similar to 23 SGR1-OX plants, confirming that NAC016 directly activates SGR1 expression in the leaf 24 senescence regulatory cascade. Although we found that NAC016 activates SGR1 expression in 25 senescing leaves, this transcriptional regulation is considerably weaker in maturing seeds; the 26 seeds of sgr1-1 mutants (also known as nonyellowing1-1, nye1-1) stayed green, while the seeds of 27 nac016-1 mutants turned from green to yellow normally. We also found that the abscisic acid (ABA) 28 signaling-related transcription factor genes ABI5 and EEL and the ABA biosynthesis gene AAO3, 29 which activate SGR1 expression directly or indirectly, were significantly downregulated in nac016-1 30 mutants and upregulated in NAC016-OX plants. Howeve...

show abstract

A coherent feedforward loop design principle to sustain robustness of biological networks

Cited by 37 publications

References 49 publications

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

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

PIF1-Interacting Transcription Factors and Their Binding Sequence Elements Determine the in Vivo Targeting Sites of PIF1

Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription

Contact Info

Product

Resources

About