HISTONE DEACETYLASE 9 stimulates auxin-dependent thermomorphogenesis in Arabidopsis thaliana by mediating H2A.Z depletion

Abstract

Many plant species respond to unfavorable high ambient temperatures by adjusting their vegetative body plan to facilitate cooling. This process is known as thermomorphogenesis and is induced by the phytohormone auxin. Here, we demonstrate that the chromatin-modifying enzyme HISTONE DEACETYLASE 9 (HDA9) mediates thermomorphogenesis but does not interfere with hypocotyl elongation during shade avoidance. HDA9 is stabilized in response to high temperature and mediates histone deacetylation at the YUCCA8 locus, a rate-limiting enzyme in auxin biosynthesis, at warm temperatures. We show that HDA9 permits net eviction of the H2A.Z histone variant from nucleosomes associated with YUCCA8, allowing binding and transcriptional activation by PHYTOCHROME INTERACTING FACTOR 4, followed by auxin accumulation and thermomorphogenesis.

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

“…However, AHL22 overexpression results in short and stunted siliques and compact plants ( Yun et al , 2012 ), similar to pwr and hda9 mutants. However, unlike pwr and hda9 ( Kim et al , 2013 ; Yumul 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 ; Yang et al , 2019 ; Zeng et al , 2020 ), AHL22 overexpression leads to delayed flowering ( Yun et al , 2012 ). 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 ).…”

“…HDA9 expression is observed in several Arabidopsis organs and tissues across developmental stages, which suggests that HDA9 functions throughout the plant’s life cycle ( Van Zanten et al , 2014 ; Kang et al , 2015 ; Suzuki et al , 2018 ; Mayer et al , 2019 ; van der Woude et al , 2019 ) ( Table 1 ). In germinating seedlings, HDA9 is mainly present in below-ground parts and the root–hypocotyl junction ( Van Zanten et al , 2014 ; van der Woude et al , 2019 ), and the gene becomes more ubiquitously expressed later in development ( Hollender and Liu, 2008 ; Kang et al , 2015 ; Mayer et al , 2019 ). Accordingly, the Brassica juncea HDA9 homolog ( BjuHDA9 ) is ubiquitously detected throughout the plant and particularly in floral tissues ( Yan et al , 2018 ).…”

“…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 ).…”

“…1 ; Table 2 ). Moreover, HDA9 mediates responses to environmental signals such as salt, drought ( Zheng et al , 2016 ; Baek et al , 2020 ; Khan et al , 2020 ; Zheng et al , 2020 ), and warm temperatures ( Tasset et al , 2018 ; Shen et al , 2019 ; van der Woude et al , 2019 ).…”