Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land

Zhao, Chenchen; Wang, Yuanyuan; Chan, Kai Xun; Marchant, Dominique; Franks, Peter J.; Randall, David; Tee, Estee E-Ling; Chen, Guang; Ramesh, Sunita A.; Phua, Su Yin; Zhang, Ben; Hills, Adrian; Dai, Fei; Xue, Dawei; Gilliham, Matthew; Tyerman, Stephen D.; Nevo, Eviatar; Wu, Feibo; Zhang, Guoping; Wong, Gane Ka‐Shu; Leebens‐Mack, James H.; Melkonian, Michael; Blatt, Michael R.; Soltis, Pamela S.; Soltis, Douglas E.; Pogson, Barry J.; Chen, Zhonghua

doi:10.1073/pnas.1812092116

Cited by 128 publications

(123 citation statements)

References 53 publications

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“…Light-induced metabolic adjustments, beyond photosynthetic carbon metabolism and other chloroplastic pathways, in turn remain poorly understood. Recently, Zhao et al (2019) demonstrated that a conserved signaling mechanism, where a chloroplast retrograde signal interacts with hormonal signaling to drive stomatal closure, is operational in angiosperms, mosses and ferns [48]. Our studies provide evidence that high-light-induced signals, likely originating from chloroplasts, are reflected by regulatory adjustments in SAHH at the level of complex formation and phosphorylation in both Physcomitrella and Arabidopsis (Fig 5A).…”

Section: Discussionsupporting

confidence: 62%

Evolutionary conservation and multilevel post-translational control of S-adenosyl-homocysteine-Hydrolase in land plants

Alegre¹,

Pascual²,

Trotta³

et al. 2019

Preprint

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22Trans-methylation reactions are intrinsic to cellular metabolism in all living organisms. In land 23 plants, a range of substrate-specific methyltransferases catalyze the methylation of DNA, RNA, 24 proteins, cell wall components and numerous species-specific metabolites, thereby providing 25 means for growth and acclimation in various terrestrial habitats. Trans-methylation reactions 26 consume vast amounts of S-adenosyl-L-methionine (SAM) as a methyl donor in several 27 cellular compartments. The inhibitory reaction by-product, S-adenosyl-L-homocysteine 28 (SAH), is continuously removed by SAH hydrolase (SAHH) activity, and in doing so 29 essentially maintains trans-methylation reactions in all living cells. Here we report on the 30 evolutionary conservation and multilevel post-translational control of SAHH in land plants. 31 We find that SAHH forms oligomeric protein complexes in phylogenetically divergent land 32 plants, and provide evidence that the predominant enzyme is a tetramer. By analyzing light-33 stress-induced adjustments occurring on SAHH in Arabidopsis thaliana and Physcomitrella 34 patens, we demonstrate that both angiosperms and bryophytes undergo regulatory adjustments 35 in the levels of protein complex formation and post-translational modification of this 36 metabolically central enzyme. Collectively, these data suggest that plant adaptation to 37 terrestrial environments involved evolution of regulatory mechanisms that adjust the trans-38 methylation machinery in response to environmental cues. 39 40 41 3 42 INTRODUCTION 43 Land plants have evolved sophisticated biochemical machineries that support cell metabolism, 44 growth and acclimation in various terrestrial habitats. One of the most common biochemical 45 modification occurring on biological molecules is methylation, which is typical for DNA, 46 RNA, proteins, and a vast range of metabolites. Trans-methylation reactions are therefore 47 important in a relevant number of metabolic and regulatory interactions, which determine 48 physiological processes during the entire life cycle of plants. Trans-methylation reactions are 49 carried out by methyl transferases (MTs), which can be classified into O-MTs, N-MTs, C-MTs 50 and S-MTs based on the atom that hosts the methyl moiety [1,2]. All these enzymes require S-51 adenosyl-L-methionine (SAM) as a methyl donor [3]. Among MTs, O-MTs form a large group 52 of substrate-specific enzymes capable of methylating RNA, proteins, pectin, monolignols as 53 well as various small molecules in various cellular compartments [2]. 54 55 The availability of SAM is a prerequisite for methylation, while the methylation reaction by-56 product, S-adenosyl-L-homocysteine (SAH) is a potent inhibitor of MT activity and must 57 therefore be efficiently removed [4]. To ensure the maintenance of SAM-dependent trans-58 methylation capacity, SAH is rapidly hydrolysed by S-adenosyl-L-homocysteine hydrolase 59 (SAHH, EC 3.3.1.1) in a reaction that yields L-homocysteine (HCY) and adenosine (ADO) 60 [5]. Subsequent...

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Section: Discussionsupporting

confidence: 62%

Evolutionary conservation and multilevel post-translational control of S-adenosyl-homocysteine-Hydrolase in land plants

Alegre¹,

Pascual²,

Trotta³

et al. 2019

Preprint

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“…responses in which guard cell volume and hence stomatal aperture are driven by actively mediated changes in guard cell osmotic content). Seedless plants clearly possess actively mediated responses to light (Doi et al ., ), CO 2 (Franks & Britton‐Harper, ), and drought and high‐light stress (Zhao et al ., ), although the generality of active stomatal movements in some bryophytes remains unclear (Renzaglia et al ., ; Duckett & Pressel, ; Duckett et al ., ).…”

Section: New Ideas and New Evidence About Stomatal Responses To Watermentioning

confidence: 99%

How do stomata respond to water status?

2019

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Summary Stomatal responses to humidity, soil moisture and other factors that influence plant water status are critical drivers of photosynthesis, productivity, water yield, ecohydrology and climate forcing, yet we still lack a thorough mechanistic understanding of these responses. Here I review historical and recent advances in stomatal water relations. Clear evidence now implicates a metabolically mediated response to leaf water status (‘hydroactive feedback’) in stomatal responses to evaporative demand and soil drought, possibly involving abscisic acid production in leaves. Other hypothetical mechanisms involving vapor and heat transport within leaves may contribute to humidity, light and temperature responses, but require further theoretical clarification and experimental validation. Variation and dynamics in hydraulic conductance, particularly within leaves, may contribute to water status responses. Continuing research to fully resolve mechanisms of stomatal responses to water status should focus on several areas: validating and quantifying the mechanism of leaf‐based hydroactive feedback, identifying where in leaves water status is actively sensed, clarifying the role of leaf vapor and energy transport in humidity and temperature responses, and verifying foundational but minimally replicated results of stomatal hydromechanics across species. Clarity on these matters promises to deliver modelers with a tractable and reliable mechanistic model of stomatal responses to water status.

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“…Homologues of genes once thought to be restricted to embryophytes are now being detected in streptophyte algae. Examples include those involved in symbiotic or pathogenic interactions with soil microbes 4 , phytohormone signalling [5][6][7][8] , desiccation/stress 9 , plastid/nucleus retrograde signalling 10,11 and cell wall metabolism 12 . Importantly, many transcription factors (TFs) thought to be specific to embryophytes originated in streptophyte algae and also substantially expanded there 13 .…”

mentioning

confidence: 99%

Genomes of early-diverging streptophyte algae shed light on plant terrestrialization

et al. 2019

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Mounting evidence suggests that terrestrialization of plants started in streptophyte green algae, favoured by their dual existence in freshwater and subaerial/terrestrial environments. Here, we present the genomes of Mesostigma viride and Chlorokybus atmophyticus, two sister taxa in the earliest-diverging clade of streptophyte algae dwelling in freshwater and subaerial/terrestrial environments, respectively. We provide evidence that the common ancestor of M. viride and C. atmophyticus (and thus of streptophytes) had already developed traits associated with a subaerial/terrestrial environment, such as embryophyte-type photorespiration, canonical plant phytochrome, several phytohormones and transcription factors involved in responses to environmental stresses, and evolution of cellulose synthase and cellulose synthase-like genes characteristic of embryophytes. Both genomes differed markedly in genome size and structure, and in gene family composition, revealing their dynamic nature, presumably in response to adaptations to their contrasting environments. The ancestor of M. viride possibly lost several genomic traits associated with a subaerial/terrestrial environment following transition to a freshwater habitat.

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Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land

Cited by 128 publications

References 53 publications

Evolutionary conservation and multilevel post-translational control of S-adenosyl-homocysteine-Hydrolase in land plants

Evolutionary conservation and multilevel post-translational control of S-adenosyl-homocysteine-Hydrolase in land plants

How do stomata respond to water status?

Genomes of early-diverging streptophyte algae shed light on plant terrestrialization

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