scholarly journals Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage

2017 ◽  
Author(s):  
Philip Carella ◽  
Anna Gogleva ◽  
Marta Tomaselli ◽  
Carolin Alfs ◽  
Sebastian Schornack
Keyword(s):  
Specific Interaction ◽  
Land Plant ◽  
Land Plants ◽  
Phytophthora Palmivora ◽  
Marchantia Polymorpha ◽  
Broad Host Range ◽  
Tissue Specific ◽  
Plant Trait ◽  
Oomycete Pathogen ◽  
Eukaryotic Microbes

ABSTRACTThe expansion of plants onto land was a formative event that brought forth profound changes to the Earth’s geochemistry and biota. Filamentous eukaryotic microbes developed the ability to colonize plant tissues early during the evolution of land plants, as demonstrated by intimate symbiosis-like associations in >400 million-year-old fossils. However, the degree to which filamentous microbes establish pathogenic interactions with early divergent land plants is unclear. Here, we demonstrate that the broad host-range oomycete pathogen Phytophthora palmivora colonizes liverworts, the earliest divergent land plant lineage. We show that P. palmivora establishes a complex tissue-specific interaction with Marchantia polymorpha, where it completes a full infection cycle within air chambers of the dorsal photosynthetic layer. Remarkably, P. palmivora invaginates M. polymorpha cells with haustoria-like structures that accumulate host cellular trafficking machinery and the membrane-syntaxin MpSYP13B but not the related MpSYP13A. Our results indicate that the intracellular accommodation of filamentous microbes is an ancient plant trait that is successfully exploited by pathogens like P. palmivora.

scholarly journals Phytophthora palmivora establishes tissue-specific intracellular infection structures in the earliest divergent land plant lineage

2018 ◽  
Vol 115 (16) ◽  
pp. E3846-E3855 ◽  
Author(s):  
Philip Carella ◽  
Anna Gogleva ◽  
Marta Tomaselli ◽  
Carolin Alfs ◽  
Sebastian Schornack
Keyword(s):  
Specific Interaction ◽  
Land Plant ◽  
Land Plants ◽  
Phytophthora Palmivora ◽  
Marchantia Polymorpha ◽  
Broad Host Range ◽  
Tissue Specific ◽  
Plant Trait ◽  
Oomycete Pathogen ◽  
Eukaryotic Microbes

The expansion of plants onto land was a formative event that brought forth profound changes to the earth’s geochemistry and biota. Filamentous eukaryotic microbes developed the ability to colonize plant tissues early during the evolution of land plants, as demonstrated by intimate, symbiosis-like associations in >400 million-year-old fossils. However, the degree to which filamentous microbes establish pathogenic interactions with early divergent land plants is unclear. Here, we demonstrate that the broad host-range oomycete pathogen Phytophthora palmivora colonizes liverworts, the earliest divergent land plant lineage. We show that P. palmivora establishes a complex tissue-specific interaction with Marchantia polymorpha, where it completes a full infection cycle within air chambers of the dorsal photosynthetic layer. Remarkably, P. palmivora invaginates M. polymorpha cells with haustoria-like structures that accumulate host cellular trafficking machinery and the membrane syntaxin MpSYP13B, but not the related MpSYP13A. Our results indicate that the intracellular accommodation of filamentous microbes is an ancient plant trait that is successfully exploited by pathogens like P. palmivora.

scholarly journals Deep evolutionary origin of gamete-directed zygote activation by KNOX/BELL transcription factors in green plants

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Tetsuya Hisanaga ◽  
Shota Fujimoto ◽  
Yihui Cui ◽  
Katsutoshi Sato ◽  
Ryosuke Sano ◽  
...  
Keyword(s):  
Arabidopsis Thaliana ◽  
Transcription Factors ◽  
Chlamydomonas Reinhardtii ◽  
Plant Species ◽  
Land Plant ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Mating Types ◽  
Meristem Maintenance

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.

scholarly journals Deep evolutionary origin of gamete-directed zygote activation by KNOX/BELL transcription factors in green plants

2020 ◽  
Author(s):  
Tetsuya Hisanaga ◽  
Shota Fujimoto ◽  
Yihui Cui ◽  
Katsutoshi Sato ◽  
Ryosuke Sano ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Chlamydomonas Reinhardtii ◽  
Plant Species ◽  
Green Alga ◽  
Land Plant ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Mating Types ◽  
Meristem Maintenance

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.

scholarly journals Regulation of the Poly(A) Status of Mitochondrial mRNA by Poly(A)-Specific Ribonuclease Is Conserved among Land Plants

2019 ◽  
Vol 61 (3) ◽  
pp. 470-480
Author(s):  
Mai Kanazawa ◽  
Yoko Ikeda ◽  
Ryuichi Nishihama ◽  
Shohei Yamaoka ◽  
Nam-Hee Lee ◽  
...  
Keyword(s):  
Molecular Genetic ◽  
Regulatory System ◽  
Land Plant ◽  
Molecular Genetic Analysis ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Mitochondrial Rna ◽  
Cellular Functions ◽  
The Stability

Abstract Regulation of the stability and the quality of mitochondrial RNA is essential for the maintenance of mitochondrial and cellular functions in eukaryotes. We have previously reported that the eukaryotic poly(A)-specific ribonuclease (PARN) and the prokaryotic poly(A) polymerase encoded by AHG2 and AGS1, respectively, coordinately regulate the poly(A) status and the stability of mitochondrial mRNA in Arabidopsis. Mitochondrial function of PARN has not been reported in any other eukaryotes. To know how much this PARN-based mitochondrial mRNA regulation is conserved among plants, we studied the AHG2 and AGS1 counterparts of the liverwort, Marchantia polymorpha, a member of basal land plant lineage. We found that M. polymorpha has one ortholog each for AHG2 and AGS1, named MpAHG2 and MpAGS1, respectively. Their Citrine-fused proteins were detected in mitochondria of the liverwort. Molecular genetic analysis showed that MpAHG2 is essential and functionally interacts with MpAGS1 as observed in Arabidopsis. A recombinant MpAHG2 protein had a deadenylase activity in vitro. Overexpression of MpAGS1 and the reduced expression of MpAHG2 caused an accumulation of polyadenylated Mpcox1 mRNA. Furthermore, MpAHG2 suppressed Arabidopsis ahg2-1 mutant phenotype. These results suggest that the PARN-based mitochondrial mRNA regulatory system is conserved in land plants.

scholarly journals Neofunctionalisation of basic helix loop helix proteins occurred when plants colonised the land

2019 ◽  
Author(s):  
Clémence Bonnot ◽  
Alexander J. Hetherington ◽  
Clément Champion ◽  
Holger Breuninger ◽  
Steven Kelly ◽  
...  
Keyword(s):  
Single Cells ◽  
Root Hairs ◽  
Land Plant ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Last Common Ancestor ◽  
Single Class ◽  
Basic Helix Loop Helix ◽  
Helix Loop Helix ◽  
Class Viii

ABSTRACTROOT HAIR DEFECTIVE SIX-LIKE (RSL) genes control the development of structures – rhizoids, root hairs, gemmae, mucilage papillae – that develop from single cells at the surface of diverse groups of land plants. RSL proteins constitute a subclass (VIIIc) of the basic helix loop helix (bHLH) class VIII transcription factor family. We set out to determine if the function of RSL genes in the control of cell differentiation in land plants was inherited from streptophyte algal ancestor. The Charophyceae are a monophyletic class of streptophyte algae with tissue-like structures and rhizoids. We identified the single class VIII bHLH gene from the charophyceaen alga Chara braunii (CbbHLHVIII). Phylogenetic analysis suggests that this protein is sister to the RSL (bHLH subclass VIIIc) proteins and together they constitute a monophyletic group. Expression of CbbHLHVIII does not compensate for loss of the RSL function in either Marchantia polymorpha or Arabidopsis thaliana. Furthermore, CbbHLHVIII is expressed at sites of morphogenesis in C. braunii – the apices, nodes and gametangia – but not in rhizoids. This indicates that C. braunii class VIII protein is functionally different from land plant RSL proteins; they control rhizoid development in land plants but not in the charophycean algae. These data are consistent with the hypothesis that RSL proteins and their function in the differentiation of cells at the plant surface evolved in the lineage leading to land plants after the divergence of the land plants and C. braunii from their last common ancestor. This may have occurred by neofunctionalisation at or before the colonisation of the land by streptophytes.

scholarly journals Auronidins are a previously unreported class of flavonoid pigments that challenges when anthocyanin biosynthesis evolved in plants

2019 ◽  
Vol 116 (40) ◽  
pp. 20232-20239 ◽  
Author(s):  
Helge Berland ◽  
Nick W. Albert ◽  
Anne Stavland ◽  
Monica Jordheim ◽  
Tony K. McGhie ◽  
...  
Keyword(s):  
Anthocyanin Biosynthesis ◽  
Extreme Environments ◽  
Land Plant ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Red Cell ◽  
Evolutionary Transition ◽  
Model Species ◽  
Harmful Effects ◽  
Early Land

Anthocyanins are key pigments of plants, providing color to flowers, fruit, and foliage and helping to counter the harmful effects of environmental stresses. It is generally assumed that anthocyanin biosynthesis arose during the evolutionary transition of plants from aquatic to land environments. Liverworts, which may be the closest living relatives to the first land plants, have been reported to produce red cell wall-bound riccionidin pigments in response to stresses such as UV-B light, drought, and nutrient deprivation, and these have been proposed to correspond to the first anthocyanidins present in early land plant ancestors. Taking advantage of the liverwort model species Marchantia polymorpha, we show that the red pigments of Marchantia are formed by a phenylpropanoid biosynthetic branch distinct from that leading to anthocyanins. They constitute a previously unreported flavonoid class, for which we propose the name “auronidin,” with similar colors as anthocyanin but different chemistry, including strong fluorescence. Auronidins might contribute to the remarkable ability of liverworts to survive in extreme environments on land, and their discovery calls into question the possible pigment status of the first land plants.

scholarly journals Identification of a divergent basal body assembly protein involved in land plant spermatogenesis

2021 ◽  
Author(s):  
Shizuka Koshimizu ◽  
Naoki Minamino ◽  
Tomoaki Nishiyama ◽  
Emiko Yoro ◽  
Kazuo Ebine ◽  
...  
Keyword(s):  
Basal Body ◽  
Molecular Mechanisms ◽  
Molecular Genetic ◽  
Male Gamete ◽  
Multilayered Structure ◽  
Land Plant ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Uppermost Layer ◽  
Computational Analyses

Oogamy is a form of sexual reproduction and evolved independently in animals, fungi, and plants. In streptophyte plants, Charophyceae, Coleochaetophyceae, bryophytes, lycophytes, ferns (monilophytes), and some gymnosperms (Cycads and Ginkgo) utilize spermatozoids as the male gamete. Plant spermatozoids commonly possess characteristic structures such as the spline, which consists of a microtubule array, the multilayered structure (MLS) in which the uppermost layer is continuum of the spline, and multiple flagella. However, the molecular mechanisms underpinning plant spermatogenesis remain to be elucidated. To identify the genes involved in plant spermatogenesis, we performed computational analyses and successfully found deeply divergent BLD10s by combining multiple methods and omics-data. We then validated the functions of candidate genes in the liverwort Marchantia polymorpha and the moss Physcomitrium patens and found that MpBLD10 and PpBLD10 are required for normal basal body and flagella formation. Mpbld10 mutants exhibited defects in remodeling of the cytoplasm and nucleus during spermatozoid formation, thus MpBLD10 should be involved in chromatin reorganization and elimination of the cytoplasm during spermiogenesis. Streptophyte BLD10s are orthologous to BLD10/CEP135 family proteins, which function in basal body assembly, but we found that BLD10s evolved especially fast in land plants and MpBLD10 might obtain additional functions in spermatozoid formation through the fast molecular evolution. This study provides a successful example of combinatorial study from evolutionary and molecular genetic perspectives that elucidated a function of the key protein of the basal body formation that fast evolved in land plants.

scholarly journals Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress

PeerJ ◽  
2021 ◽  
Vol 9 ◽  
pp. e12419
Author(s):  
Totan Kumar Ghosh ◽  
Naznin Haque Tompa ◽  
Md. Mezanur Rahman ◽  
Mohammed Mohi-Ud-Din ◽  
S. M. Zubair Al-Meraj ◽  
...  
Keyword(s):  
Oxidative Stress ◽  
Antioxidant Enzymes ◽  
Abscisic Acid ◽  
Drought Tolerance ◽  
Osmotic Stress ◽  
Photosynthetic Pigment ◽  
Land Plant ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Key Species

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.

scholarly journals Independent evolution of lateral inhibition mechanisms in different lineages of land plants: MpFEW RHIZOIDS1 miRNA-mediated lateral inhibition controls rhizoid cell patterning in Marchantia polymorpha

2019 ◽  
Author(s):  
Anna Thamm ◽  
Timothy E Saunders ◽  
Liam Dolan
Keyword(s):  
Lateral Inhibition ◽  
Land Plant ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Bhlh Transcription Factor ◽  
Two Dimensional ◽  
Loss Of Function ◽  
Wild Type ◽  
Helix Loop Helix ◽  
Differentiated Cells

ABSTRACTLateral inhibition patterns differentiated cells during development in bacteria, metazoans and land plants. Tip-growing rhizoid cells develop among flat epidermal cells in the epidermis of the early diverging land plant Marchantia polymorpha. We show that the majority of rhizoid cells develop individually but some develop in linear, one-dimensional clusters of between two and seven rhizoid cells in wild type plants. The distribution of rhizoid cells can be accounted for within a simple model of lateral inhibition. The model also predicted that, in the absence of lateral inhibition, rhizoid cell clusters would be two-dimensional with larger clusters than those formed with lateral inhibition. Rhizoid differentiation in Marchantia polymorpha is positively regulated by the ROOT HAIR DEFECTIVE SIX-LIKE1 (MpRSL1) basic Helix Loop Helix (bHLH) transcription factor which is directly repressed by the FEW RHIZOIDS1 (MpFRH1) miRNA. To test if MpFRH1 miRNA acts during lateral inhibition we generated loss-of-function mutants that did not produce the MpFRH1 miRNA. Two-dimensional clusters of rhizoids develop in Mpfrh1loss-of-function (lof) mutants as predicted by the model for plants that lack lateral inhibition. Furthermore, clusters of up to nine rhizoid cells developed in the Mpfrh1lof mutants compared to a maximum number of seven observed in wild type. The higher steady state levels of MpRSL1 mRNA in Mpfrh1lof mutants indicate that MpFRH1-mediated lateral inhibition involves the repression of MpRSL1 activity. Together the modelling and genetic data indicate that the pattern of cell differentiation in the M. polymorpha epidermis is consistent with a lateral inhibition process in which MpFRH1 miRNA represses MpRSL1. This discovery suggests that novel mechanisms of lateral inhibition may operate in different lineages of land plants, unlike metazoans where the conserved Delta-Notch signaling system controls lateral inhibition in diverse metazoan lineages.

scholarly journals Negative regulation of conserved RSL class I bHLH transcription factors evolved independently among land plants

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Suvi Honkanen ◽  
Anna Thamm ◽  
Mario A Arteaga-Vazquez ◽  
Liam Dolan
Keyword(s):  
Transcription Factors ◽  
Root Hairs ◽  
Land Plant ◽  
Feedback Mechanism ◽  
Plant Evolution ◽  
Land Plants ◽  
Class I ◽  
Marchantia Polymorpha ◽  
Helix Loop Helix ◽  
Bhlh Transcription Factors

Basic helix-loop-helix transcription factors encoded by RSL class I genes control a gene regulatory network that positively regulates the development of filamentous rooting cells – root hairs and rhizoids – in land plants. The GLABRA2 transcription factor negatively regulates these genes in the angiosperm Arabidopsis thaliana. To find negative regulators of RSL class I genes in early diverging land plants we conducted a mutant screen in the liverwort Marchantia polymorpha. This identified FEW RHIZOIDS1 (MpFRH1) microRNA (miRNA) that negatively regulates the RSL class I gene MpRSL1. The miRNA and its mRNA target constitute a feedback mechanism that controls epidermal cell differentiation. MpFRH1 miRNA target sites are conserved among liverwort RSL class I mRNAs but are not present in RSL class I mRNAs of other land plants. These findings indicate that while RSL class I genes are ancient and conserved, independent negative regulatory mechanisms evolved in different lineages during land plant evolution.

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