HY5-HDA9 Module Transcriptionally Regulates Plant Autophagy in Response to Light-to-Dark Conversion and Nitrogen Starvation

Abstract

Light is arguably one of the most important environmental factors that determines virtually all aspects of plant growth and development, but the molecular link between light signaling and the autophagy pathway has not been elucidated in plants. In this study, we demonstrate that autophagy is activated during light-todark conversion though transcriptional upregulation of autophagy-related genes (ATGs). We showed that depletion of the ELONGATED HYPOCOTYL 5 (HY5), a key component of light signaling, leads to enhanced autophagy activity and resistance to extended darkness and nitrogen starvation treatments, contributing to higher expression of ATGs. HY5 interacts with and recruits HISTONE DEACETYLASE 9 (HDA9) to ATG5 and ATG8e loci to repress their expression by deacetylation of the Lys9 and Lys27 of histone 3. Furthermore, we found that both darkness and nitrogen depletion induce the degradation of HY5 via 26S proteasome and the concomitant disassociation of HDA9 from ATG5 and ATG8e loci, leading to their depression and thereby activated autophagy. Genetic analysis further confirmed that HY5 and HDA9 act synergistically and function upstream of the autophagy pathway. Collectively, our study unveils a previously unknown transcriptional and epigenetic network that regulates autophagy in response to light-to-dark conversion and nitrogen starvation in plants.

SINAT E3 ligases regulate the stability of the ESCRT component FREE1 in response to iron deficiency in plants

“…Cytosolic materials can be encapsulated and delivered to the vacuole/lysosome via the macroautophagy (hereafter referred to as autophagy) pathway. In macroautophagy, a double membrane-bound structure termed the autophagosome forms, which engulfs cargo proteins or organelles for subsequent delivery to the vacuolar lumen for proteolysis, or induces hydrolysis upon fusion between the autophagosome and vacuole/lysosome (Li and Vierstra 2012;Marshall and Vierstra 2018;Zhuang et al 2018;Yang et al 2020aYang et al , 2020b. Besides the autophagy pathway, another system that recognizes and delivers ubiquitinated cargo to the vacuole is the multivesicular body (MVB)-mediated endosomal sorting pathway, which is regulated by the endosomal sorting complex required for transport (ESCRT) complex.…”

The diverse and unanticipated roles of histone deacetylase 9 in coordinating plant development and environmental acclimation

“…Furthermore, afr1 and afr2 mutants exhibit elongated petioles and an open rosette structure, which is in contrast to the stunted hda9 mutant phenotype ( Gu et al , 2013 ), whereas similarly to hda9 and pwr , the afr mutants exhibit early flowering ( Gu et al , 2013 ). Additional proteins shown to interact with HDA9 include ASG2 ( Ducos et al , 2017 ), EARLY FLOWERING3 (ELF3), and possibly LUX ARRHYTHMO (LUX) ( Lee et al , 2019 ; Park et al , 2019 ), VP1/ABI3-LIKE 1 (VAL1) and VAL2 ( Zeng et al , 2020 ), ELONGATED HYPOCOTYL 5 (HY5) ( Yang et al , 2020 ), and ABA INSENSITIVE4 (ABI4) and ABI3 ( Baek et al , 2020 , Khan et al , 2020 ). These interactions are discussed below ( Fig.…”

“…The transcription factors WRKY53 ( Chen et al , 2016 ; Zheng et al , 2020 ), ABI4, ABI3 ( Baek et al , 2020 , Khan et al , 2020 ), and HY5 ( Yang et al , 2020 ), the epigenome readers VP1/ABI3-LIKE 1 (VAL1) and VAL2 ( Zeng et al , 2020 ), the circadian clock Evening Complex (EC) transcription factor(s) ELF3 and possibly LUX ( Lee et al , 2019 ; Park et al , 2019 ), and AT-hook motif-containing protein AHL22 ( Yun et al , 2012 ) are currently the only confirmed HDA9-interacting proteins with DNA binding capacity ( Fig. 1 ).…”

“…HDA9 substrates include H3K9Ac, H3K14Ac, H3K18Ac, H3K27Ac, H3K36Ac, and H3K56Ac ( Kim et al , 2013 ; Van Zanten et al , 2014 ; Kang et al , 2015 ; Chen et al , 2016 ; Kim et al , 2016 ; Mayer et al , 2019 ; Park et al , 2019 ; van der Woude et al , 2019 ; Yang et al , 2020 ; Zeng et al , 2020 ; Zheng et al , 2020 ), but not H4 or H2A lysines ( Kim et al , 2016 ; Mayer et al , 2019 ). In addition, hda9 mutants display altered H3K9Me1, H3K9Me2, H3K27Me1, H3K27Me2, and H3K36Me2 levels ( Chen et al , 2016 ; Kim et al , 2016 ; Mayer et al , 2019 ; Zeng et al , 2020 ).…”

“…On the phenotypic level ( Fig. 1 ), HDA9 regulates diverse traits including seed dormancy ( Van Zanten et al , 2014 ; Baek et al , 2020 ), flowering time ( Kim et al , 2013 ; Kang et al , 2015 ; Kim et al , 2016 ; Mayer et al , 2019 ; Park et al , 2019 ; van der Woude et al , 2019 ; Zeng et al , 2020 ), leaf senescence ( Chen et al , 2016 ; Mayer et al , 2019 ; Yang et al , 2020 ), cellular differentiation ( Lee et al , 2016 ), cell proliferation ( Suzuki et al , 2018 ), suppression of stem cuticular wax crystal accumulation ( Wang et al , 2018 ), flower opening, petal and sepal attachment to the receptacles ( Kang et al , 2015 ), and several other developmental and physiological phenotypes ( Fig. 1 ; Table 2 ).…”