Poplar acetylome profiling reveals lysine acetylation dynamics in seasonal bud dormancy release

Abstract

For perennials in boreal and temperate ecosystems, bud dormancy is crucial for survival in harsh winter. Dormancy is released by prolonged exposure to low temperatures and is followed by reactive growth in the spring. Lysine acetylation (Kac) is one of the major post-translational modifications (PTMs) that are involved in plant response to environmental signals. However, little information is available on the effects of Kac modification on bud dormancy release. Here, we report the dynamics of lysine acetylome in hybrid poplar (Populus tremula × Populus alba) dormant buds. A total of 7,594 acetyl-sites from 3,281 acetyl-proteins were identified, representing a large dataset of lysine acetylome in plants. Of them, 229 proteins were differentially acetylated during bud dormancy release and were mainly involved in the primary metabolic pathways. Site-directed mutagenesis enzymatic assays showed that Kac strongly modified the activities of two key enzymes of primary metabolism, pyruvate dehydrogenase (PDH) and isocitrate dehydrogenase (IDH). We thus propose that Kac of enzymes could be an important strategy for reconfiguration of metabolic processes during bud dormancy release. In all, our results reveal the importance of Kac in bud dormancy release and provide a new perspective to understand the molecular mechanisms of seasonal growth of trees.

Advances in proteome-wide analysis of plant lysine acetylation

“…tremula × P . alba , there was a slight decrease in LysAc during dormancy release ( Liao et al., 2021 ). Within 0–48 h after imbibition of O .…”

“…(2011) localized Lys-acetylated proteins to the nucleus, plasma membrane, and chloroplast, whereas the chromocenter was hypo-Lys-acetylated. Subcellular localization predictions reveal that the number of Lys-acetylated proteins varies across subcellular compartments among plant species, tissues, and developmental stages ( Fang et al., 2015 ; He et al., 2016 ; Xia et al., 2016 ; Xiong et al., 2016 ; Zhang et al., 2016 ; Zhen et al., 2016 ; Chen et al., 2018 ; Jiang et al., 2018 ; Li et al., 2018b , 2021b ; Meng et al., 2018 ; Xue et al., 2018 ; Zhou et al., 2018 ; Zhu et al., 2018 ; Cao et al., 2019 ; Yan et al., 2020 ; Liao et al., 2021 ) ( Figure 2 B). Almost 90% of Lys-acetylated proteins are located in the chloroplast, cytoplasm, nucleus, and mitochondria of plant cells.…”

“…tremula × P . alba ( Liao et al., 2021 ). Numerous enzymes that participate in the degradation of lipids and amino acids to produce energy for bud breakage are differentially Lys-acetylated during bud break ( Liao et al., 2021 ).…”

“…alba ( Liao et al., 2021 ). Numerous enzymes that participate in the degradation of lipids and amino acids to produce energy for bud breakage are differentially Lys-acetylated during bud break ( Liao et al., 2021 ). Therefore, LysAc of histones, signal effectors, and key metabolic enzymes plays important roles in germination signaling pathways and reconfiguration of the metabolic system.…”

“…To date, plant Lys-acetylproteome analyses have focused mainly on higher plants, including A . thaliana ( Finkemeier et al., 2011 ; Wu et al., 2011 ; Koenig et al., 2014 ; Hartl et al., 2017 ; Uhrig et al., 2017 ; Liu et al., 2018 ; Koskela et al., 2018 ; Bienvenut et al., 2020 ), Vitis vinifera ( Melo-Braga et al., 2012 ; Liu et al., 2019 ), Pisum sativum ( Smith-Hammond et al., 2014a ), Glycine max ( Smith-Hammond et al., 2014b ; Li et al., 2021a ), Oryza sativa ( Nallamilli et al., 2014 ; He et al., 2016 ; Xiong et al., 2016 ; Wang et al., 2017 ; Li et al., 2018a , 2018b ; Meng et al., 2018 ; Xue et al., 2018 ; Zhou et al., 2018 ), Fragaria ananassa ( Fang et al., 2015 ), Medicago truncatula ( Marx et al., 2016 ), Triticum aestivum ( Zhang et al., 2016 ; Zhu et al., 2018 ; Guo et al., 2020 ), Brachypodium distachyon ( Zhen et al., 2016 ), Picea asperata ( Xia et al., 2016 ), Camellia sinensis ( Xu et al., 2017 ; Jiang et al., 2018 ), Zea mays ( Walley et al., 2018 ; Yan et al., 2020 ), Kandelia candel ( Pan et al., 2018 ), Gossypium hirsutum ( Singh et al., 2020 ), Hibiscus cannabinus ( Chen et al., 2019 ), Paulownia tomentosa ( Cao et al., 2019 ), Petunia hybrida ( Zhao et al., 2020 ), Nicotiana benthamiana ( Yuan et al., 2021 ), Populus tremula × Populus alba ( Liao et al., 2021 ), Broussonetia papyrifera ( Li et al., 2021b ), and Phoebe zhennan ( Zhao et al., 2021 ) ( Table 1 ). By contrast, the Lys-acetylproteomes of lower plants are poorly studied and have been documented only in Phaeodactylum tricornutum ( Chen et al., 2018 ) and ...…”