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Physiological Roles of Flavodiiron Proteins and Photorespiration in the Liverwort Marchantia polymorpha.

ABSTRACT: Against the potential risk in oxygenic photosynthesis, that is, the generation of reactive oxygen species, photosynthetic electron transport needs to be regulated in response to environmental fluctuations. One of the most important regulations is keeping the reaction center chlorophyll (P700) of photosystem I in its oxidized form in excess light conditions. The oxidation of P700 is supported by dissipating excess electrons safely to O₂, and we previously found that the molecular mechanism of the alternative electron sink is changed from flavodiiron proteins (FLV) to photorespiration in the evolutionary history from cyanobacteria to plants. However, the overall picture of the regulation of photosynthetic electron transport is still not clear in bryophytes, the evolutionary intermediates. Here, we investigated the physiological roles of FLV and photorespiration for P700 oxidation in the liverwort Marchantia polymorpha by using the mutants deficient in FLV (flv1) at different O₂ partial pressures. The effective quantum yield of photosystem II significantly decreased at 2kPa O₂ in flv1, indicating that photorespiration functions as the electron sink. Nevertheless, it was clear from the phenotype of flv1 that FLV was dominant for P700 oxidation in M. polymorpha. These data suggested that photorespiration has yet not replaced FLV in functioning for P700 oxidation in the basal land plant probably because of the lower contribution to lumen acidification, compared with FLV, as reflected in the results of electrochromic shift analysis.

SUBMITTER: Shimakawa G

PROVIDER: S-EPMC8418088 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The liverwort Marchantia polymorpha is a member of the most basal lineage of land plants (embryophytes) and likely retains many ancestral morphological, physiological and molecular characteristics. Despite its phylogenetic importance and the availability of previous EST studies, M. polymorpha's lack of economic importance limits accessible genomic resources for this species. We employed Illumina RNA-Seq technology to sequence the gametophyte transcriptome of M. polymorpha. cDNA libraries from 6 different male and female developmental tissues were sequenced to delineate a global view of the M. polymorpha transcriptome. Approximately 80 million short reads were obtained and assembled into a non-redundant set of 46,533 transcripts (> = 200 bp) from 46,070 loci. The average length and the N50 length of the transcripts were 757 bp and 471 bp, respectively. Sequence comparison of assembled transcripts with non-redundant proteins from embryophytes resulted in the annotation of 43% of the transcripts. The transcripts were also compared with M. polymorpha expressed sequence tags (ESTs), and approximately 69.5% of the transcripts appeared to be novel. Twenty-one percent of the transcripts were assigned GO terms to improve annotation. In addition, 6,112 simple sequence repeats (SSRs) were identified as potential molecular markers, which may be useful in studies of genetic diversity. A comparative genomics approach revealed that a substantial proportion of the genes (35.5%) expressed in M. polymorpha were conserved across phylogenetically related species, such as Selaginella and Physcomitrella, and identified 580 genes that are potentially unique to liverworts. Our study presents an extensive amount of novel sequence information for M. polymorpha. This information will serve as a valuable genomics resource for further molecular, developmental and comparative evolutionary studies, as well as for the isolation and characterization of functional genes that are involved in sex differentiation and sexual reproduction in this liverwort.

Project description:Liverwort Marchantia polymorpha is considered as the key species for addressing a myriad of questions in plant biology. Exploration of drought tolerance mechanism(s) in this group of land plants offers a platform to identify the early adaptive mechanisms involved in drought tolerance. The current study aimed at elucidating the drought acclimation mechanisms in liverwort's model M. polymorpha. The gemmae, asexual reproductive units of M. polymorpha, were exposed to sucrose (0.2 M), mannitol (0.5 M) and polyethylene glycol (PEG, 10%) for inducing physiological drought to investigate their effects at morphological, physiological and biochemical levels. Our results showed that drought exposure led to extreme growth inhibition, disruption of membrane stability and reduction in photosynthetic pigment contents in M. polymorpha. The increased accumulation of hydrogen peroxide and malondialdehyde, and the rate of electrolyte leakage in the gemmalings of M. polymorpha indicated an evidence of drought-caused oxidative stress. The gemmalings showed significant induction of the activities of key antioxidant enzymes, including superoxide dismutase, catalase, ascorbate peroxidase, dehydroascorbate reductase and glutathione S-transferase, and total antioxidant activity in response to increased oxidative stress under drought. Importantly, to counteract the drought effects, the gemmalings also accumulated a significant amount of proline, which coincided with the evolutionary presence of proline biosynthesis gene Δ1-pyrroline-5-carboxylate synthase 1 (P5CS1) in land plants. Furthermore, the application of exogenous abscisic acid (ABA) reduced drought-induced tissue damage and improved the activities of antioxidant enzymes and accumulation of proline, implying an archetypal role of this phytohormone in M. polymorpha for drought tolerance. We conclude that physiological drought tolerance mechanisms governed by the cellular antioxidants, proline and ABA were adopted in liverwort M. polymorpha, and that these findings have important implications in aiding our understanding of osmotic stress acclimation processes in land plants.

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Physiological Roles of Flavodiiron Proteins and Photorespiration in the Liverwort Marchantia polymorpha.

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