scholarly journals An evolutionary conserved lysine acetylation hotspot regulates plant mitochondrial malate dehydrogenase activity

2020 ◽  
Author(s):  
Manuel Balparda ◽  
Marlene Elsässer ◽  
Mariana Badia ◽  
Jonas Giese ◽  
Meike Hüdig ◽  
...  

AbstractPlants need to be able to rapidly and flexibly adjust their metabolism to changes their immediate environment. Since this necessity results from the sessile lifestyle of land plants, key mechanisms of orchestrating central metabolic acclimation are likely to have evolved early. Here we explore the role of lysine acetylation as a posttranslational modification to directly modulate metabolic function. First, we generate a lysine acetylome of the early divergent land plant Physcomitrium (Physcomitrella) patens. We identify 638 lysine acetylation sites, which were predominant in the mitochondria and plastids. A comparison with different angiosperms, including Arabidopsis thaliana, pinpoints lysine acetylation as conserved strategy in land plants. We focus on modified enzymes involved in mitochondrial central metabolism and select the mitochondrial malate dehydrogenase (mMDH), which acts as a hub of plant metabolic flexibility. In P. patens we detected a unique lysine acetylated site located next to one of the four acetylation sites detected in A. thaliana mMDH1. We assessed the kinetic behavior of recombinant A. thaliana and P. patens mMDHs with site-specifically incorporated acetyllysines. While the sites K325, K329 and K334 do not show any changes in the catalytic properties as assessed by oxaloacetate reduction activity, acetylation of A. thaliana mMDH1 at K170 markedly decreases its activity and acetylation of P. patens mMDH1 at K172 increases it. In both cases, acetylation induces modifications of the turnover number of the enzymes, without modifying the affinity for the substrates. Homology modelling of the mMDH1 proteins reveals a hotspot of lysine acetylation that is distant from the active site and homomerisation interfaces but conserved in land plants. The data reveal lysine acetylation as a strategy to tune the enzymatic properties of central metabolic enzymes with likely impact on metabolic capacity and flexibility to underpin plant acclimation.

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Tetsuya Hisanaga ◽  
Shota Fujimoto ◽  
Yihui Cui ◽  
Katsutoshi Sato ◽  
Ryosuke Sano ◽  
...  

KNOX and BELL transcription factors regulate distinct steps of diploid development in plants. In the green alga Chlamydomonas reinhardtii, KNOX and BELL proteins are inherited by gametes of the opposite mating types and heterodimerize in zygotes to activate diploid development. By contrast, in land plants such as Physcomitrium patens and Arabidopsis thaliana, KNOX and BELL proteins function in meristem maintenance and organogenesis during the later stages of diploid development. However, whether the contrasting functions of KNOX and BELL were acquired independently in algae and land plants is currently unknown. Here, we show that in the basal land plant species Marchantia polymorpha, gamete-expressed KNOX and BELL are required to initiate zygotic development by promoting nuclear fusion in a manner strikingly similar to that in C. reinhardtii. Our results indicate that zygote activation is the ancestral role of KNOX/BELL transcription factors, which shifted toward meristem maintenance as land plants evolved.


1998 ◽  
Vol 353 (1365) ◽  
pp. 113-130 ◽  
Author(s):  
Thomas J. Algeo ◽  
Stephen E. Scheckler

The Devonian Period was characterized by major changes in both the terrestrial biosphere, e.g. the evolution of trees and seed plants and the appearance of multi–storied forests, and in the marine biosphere, e.g. an extended biotic crisis that decimated tropical marine benthos, especially the stromatoporoid–tabulate coral reef community. Teleconnections between these terrestrial and marine events are poorly understood, but a key may lie in the role of soils as a geochemical interface between the lithosphere and atmosphere/hydrosphere, and the role of land plants in mediating weathering processes at this interface. The effectiveness of terrestrial floras in weathering was significantly enhanced as a consequence of increases in the size and geographic extent of vascular land plants during the Devonian. In this regard, the most important palaeobotanical innovations were (1) arborescence (tree stature), which increased maximum depths of root penetration and rhizoturbation, and (2) the seed habit, which freed land plants from reproductive dependence on moist lowland habitats and allowed colonization of drier upland and primary successional areas. These developments resulted in a transient intensification of pedogenesis (soil formation) and to large increases in the thickness and areal extent of soils. Enhanced chemical weathering may have led to increased riverine nutrient fluxes that promoted development of eutrophic conditions in epicontinental seaways, resulting in algal blooms, widespread bottomwater anoxia, and high sedimentary organic carbon fluxes. Long–term effects included drawdown of atmospheric pCO 2 and global cooling, leading to a brief Late Devonian glaciation, which set the stage for icehouse conditions during the Permo–Carboniferous. This model provides a framework for understanding links between early land plant evolution and coeval marine anoxic and biotic events, but further testing of Devonian terrestrial–marine teleconnections is needed.


2020 ◽  
Author(s):  
Tetsuya Hisanaga ◽  
Shota Fujimoto ◽  
Yihui Cui ◽  
Katsutoshi Sato ◽  
Ryosuke Sano ◽  
...  

AbstractKNOX and BELL transcription factors regulate distinct steps of diploid development in the green lineages. In the green alga Chlamydomonas reinhardtii, KNOX and BELL proteins are inherited by gametes of the opposite mating types, and heterodimerize in zygotes to activate diploid development. By contrast, in land plants such as Physcomitrella and Arabidopsis, KNOX and BELL proteins function in meristem maintenance and organogenesis during the later stages of diploid development. However, whether the contrasting functions of KNOX and BELL were acquired independently in algae and land plants is currently unknown. Here we show that in the basal land plant species Marchantia polymorpha, gamete-expressed KNOX and BELL are required to initiate zygotic development by promoting nuclear fusion in a manner strikingly similar to that of C. reinhardtii. Our results indicate that zygote activation is the ancestral role of KNOX/BELL transcription factors, which shifted toward meristem maintenance as land plants evolved.


2017 ◽  
Author(s):  
Rohan Bythell-Douglas ◽  
Carl J. Rothfels ◽  
Dennis W.D. Stevenson ◽  
Sean W. Graham ◽  
Gane Ka-Shu Wong ◽  
...  

ABSTRACTStrigolactones (SLs) are a class of plant hormones that control many aspects of plant growth. The SL signalling mechanism is homologous to that of karrikins (KARs), smoke-derived compounds that stimulate seed germination. In angiosperms, the SL receptor is an α/β hydrolase known as DWARF14 (D14); its close homologue, KARRIKIN INSENSITIVE2 (KAI2), functions as a KAR receptor, and likely recognizes an uncharacterized, endogenous signal. Previous phylogenetic analyses have suggested that the KAI2 lineage is ancestral in land plants, and that canonical D14-type SL receptors only arose in seed plants; this is paradoxical, however, as non-vascular plants synthesize and respond to SLs. Here, we have used a combination of phylogenetic and structural approaches to re-assess the evolution of the D14/KAI2 family in land plants. We analyzed 339 members of the D14/KAI2 family from land plants and charophyte algae. Our phylogenetic analyses show that the divergence between the eu-KAI2 lineage and the DDK (D14/DLK2/KAI2) lineage that includes D14 occurred very early in land plant evolution. We identify characteristic structural features of D14 and KAI2 proteins, and use homology modelling to show that the earliest members of the DDK lineage structurally resemble KAI2, and not D14 proteins. Furthermore, we show that probable SL receptors in non-seed plants do not have D14-like structure. Our results suggest that SL perception has relatively relaxed structural requirements, and that the evolution from KAI2-like to D14-like protein structure in the DDK lineage may have been driven by interactions with protein partners, rather than being required for SL perception itself.


2021 ◽  
Author(s):  
Manuel Balparda ◽  
Marlene Elsässer ◽  
Mariana B. Badia ◽  
Jonas Giese ◽  
Anastassia Bovdilova ◽  
...  

2021 ◽  
Vol 7 (1) ◽  
Author(s):  
Qiujing Yan ◽  
Liang Zhao ◽  
Wenda Wang ◽  
Xiong Pi ◽  
Guangye Han ◽  
...  

AbstractPlants harvest light energy utilized for photosynthesis by light-harvesting complex I and II (LHCI and LHCII) surrounding photosystem I and II (PSI and PSII), respectively. During the evolution of green plants, moss is at an evolutionarily intermediate position from aquatic photosynthetic organisms to land plants, being the first photosynthetic organisms that landed. Here, we report the structure of the PSI–LHCI supercomplex from the moss Physcomitrella patens (Pp) at 3.23 Å resolution solved by cryo-electron microscopy. Our structure revealed that four Lhca subunits are associated with the PSI core in an order of Lhca1–Lhca5–Lhca2–Lhca3. This number is much decreased from 8 to 10, the number of subunits in most green algal PSI–LHCI, but the same as those of land plants. Although Pp PSI–LHCI has a similar structure as PSI–LHCI of land plants, it has Lhca5, instead of Lhca4, in the second position of Lhca, and several differences were found in the arrangement of chlorophylls among green algal, moss, and land plant PSI–LHCI. One chlorophyll, PsaF–Chl 305, which is found in the moss PSI–LHCI, is located at the gap region between the two middle Lhca subunits and the PSI core, and therefore may make the excitation energy transfer from LHCI to the core more efficient than that of land plants. On the other hand, energy-transfer paths at the two side Lhca subunits are relatively conserved. These results provide a structural basis for unravelling the mechanisms of light-energy harvesting and transfer in the moss PSI–LHCI, as well as important clues on the changes of PSI–LHCI after landing.


2021 ◽  
Vol 22 (8) ◽  
pp. 4139
Author(s):  
Marina A. Romanova ◽  
Anastasiia I. Maksimova ◽  
Katharina Pawlowski ◽  
Olga V. Voitsekhovskaja

Mounting evidence from genomic and transcriptomic studies suggests that most genetic networks regulating the morphogenesis of land plant sporophytes were co-opted and modified from those already present in streptophyte algae and gametophytes of bryophytes sensu lato. However, thus far, no candidate genes have been identified that could be responsible for “planation”, a conversion from a three-dimensional to a two-dimensional growth pattern. According to the telome theory, “planation” was required for the genesis of the leaf blade in the course of leaf evolution. The key transcription factors responsible for leaf blade development in angiosperms are YABBY proteins, which until recently were thought to be unique for seed plants. Yet, identification of a YABBY homologue in a green alga and the recent findings of YABBY homologues in lycophytes and hornworts suggest that YABBY proteins were already present in the last common ancestor of land plants. Thus, these transcriptional factors could have been involved in “planation”, which fosters our understanding of the origin of leaves. Here, we summarise the current data on functions of YABBY proteins in the vegetative and reproductive development of diverse angiosperms and gymnosperms as well as in the development of lycophytes. Furthermore, we discuss a putative role of YABBY proteins in the genesis of multicellular shoot apical meristems and in the evolution of leaves in early divergent terrestrial plants.


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