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 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 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 Fundamental mechanisms of the stem cell regulation in land plants: lesson from shoot apical cells in bryophytes

2021 ◽  
Author(s):  
Yuki Hata ◽  
Junko Kyozuka
Keyword(s):  
Stem Cells ◽  
Stem Cell ◽  
Molecular Mechanisms ◽  
Cell Function ◽  
Chromatin Modification ◽  
Land Plants ◽  
Marchantia Polymorpha ◽  
Cell Regulation ◽  
Evolutionary Trajectory ◽  
Stem Cell Regulation

Abstract Key message This review compares the molecular mechanisms of stem cell control in the shoot apical meristems of mosses and angiosperms and reveals the conserved features and evolution of plant stem cells. Abstract The establishment and maintenance of pluripotent stem cells in the shoot apical meristem (SAM) are key developmental processes in land plants including the most basal, bryophytes. Bryophytes, such as Physcomitrium (Physcomitrella) patens and Marchantia polymorpha, are emerging as attractive model species to study the conserved features and evolutionary processes in the mechanisms controlling stem cells. Recent studies using these model bryophyte species have started to uncover the similarities and differences in stem cell regulation between bryophytes and angiosperms. In this review, we summarize findings on stem cell function and its regulation focusing on different aspects including hormonal, genetic, and epigenetic control. Stem cell regulation through auxin, cytokinin, CLAVATA3/EMBRYO SURROUNDING REGION-RELATED (CLE) signaling and chromatin modification by Polycomb Repressive Complex 2 (PRC2) and PRC1 is well conserved. Several transcription factors crucial for SAM regulation in angiosperms are not involved in the regulation of the SAM in mosses, but similarities also exist. These findings provide insights into the evolutionary trajectory of the SAM and the fundamental mechanisms involved in stem cell regulation that are conserved across land plants.

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 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 An Evolutionarily Conserved Coreceptor Gene Is Essential for CLAVATA Signaling in Marchantia polymorpha

2021 ◽  
Vol 12 ◽  
Author(s):  
Go Takahashi ◽  
Shigeyuki Betsuyaku ◽  
Natsuki Okuzumi ◽  
Tomohiro Kiyosue ◽  
Yuki Hirakawa
Keyword(s):  
Expression System ◽  
Molecular Genetic ◽  
Molecular Genetic Analysis ◽  
Land Plants ◽  
Peptide Ligand ◽  
Marchantia Polymorpha ◽  
Minimal Set ◽  
Cle Peptide ◽  
Evolutionarily Conserved ◽  
Specific Receptors

Growth and development of land plants are controlled by CLAVATA3/EMBRYO SURROUNDING REGION-related (CLE) family of peptide hormones. In contrast to the genetic diversity of CLE family in flowering plants, the liverwort Marchantia polymorpha possesses a minimal set of CLE, MpCLE1(TDIF homolog), and MpCLE2 (CLV3 homolog). MpCLE1 and MpCLE2 peptides exert distinct function at the apical meristem of M. polymorpha gametophyte via specific receptors, MpTDIF RECEPTOR (MpTDR) and MpCLAVATA1 (MpCLV1), respectively, both belonging to the subclass XI of leucine-rich repeat receptor-like kinases (LRR-RLKs). Biochemical and genetic studies in Arabidopsis have shown that TDR/PXY family and CLV1/BAM family recognize the CLE peptide ligand in a heterodimeric complex with a member of subclass-II coreceptors. Here we show that three LRR-RLK genes of M. polymorpha are classified into subclass II, representing three distinct subgroups evolutionarily conserved in land plants. To address the involvement of subclass-II coreceptors in M. polymorpha CLE signaling, we performed molecular genetic analysis on one of them, MpCLAVATA3 INSENSITIVE RECEPTOR KINASE (MpCIK). Two knockout alleles for MpCIK formed narrow apical meristems marked by promMpYUC2:GUS marker, which were not expanded by MpCLE2 peptide treatment, phenocopying Mpclv1. Loss of sensitivity to MpCLE2 peptide was also observed in gemma cup formation in both Mpclv1 and Mpcik. Biochemical analysis using a Nicotiana benthamiana transient expression system revealed weak association between MpCIK and MpCLV1, as well as MpCIK and MpTDR. While MpCIK may also participate in MpCLE1 signaling, our data show that the conserved CLV3-CLV1-CIK module functions in M. polymorpha, controlling meristem activity for development and organ formation for asexual reproduction.

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 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 An evolutionarily conserved coreceptor gene is essential for CLAVATA signaling in Marchantia polymorpha

2021 ◽  
Author(s):  
Go Takahashi ◽  
Shigeyuki Betsuyaku ◽  
Natsuki Okuzumi ◽  
Tomohiro Kiyosue ◽  
Yuki Hirakawa
Keyword(s):  
Expression System ◽  
Molecular Genetic ◽  
Molecular Genetic Analysis ◽  
Land Plants ◽  
Peptide Ligand ◽  
Marchantia Polymorpha ◽  
Minimal Set ◽  
Cle Peptide ◽  
Evolutionarily Conserved ◽  
Specific Receptors

AbstractGrowth and development of land plants are controlled by CLAVATA3/EMBRYO SURROUNDING REGION-related (CLE) family of peptide hormones. In contrast to the genetic diversity of CLE family in flowering plants, the liverwort Marchantia polymorpha possesses a minimal set of CLE, MpCLE1(TDIF homolog) and MpCLE2 (CLV3 homolog). MpCLE1 and MpCLE2 peptides exert distinct function at the apical meristem of M. polymorpha gametophyte via specific receptors, MpTDIF RECEPTOR (MpTDR) and MpCLAVATA1 (MpCLV1), respectively, both belonging to the subclass XI of leucine-rich repeat receptor-like kinases (LRR-RLKs). Biochemical and genetic studies in Arabidopsis have shown that TDR/PXY family and CLV1/BAM family recognize the CLE peptide ligand in a heterodimeric complex with a member of subclass-II coreceptors. Here we show that three LRR-RLK genes of M. polymorpha are classified into subclass II, representing three distinct subgroups evolutionarily conserved in land plants. To address the involvement of subclass-II coreceptors in M. polymorpha CLE signaling, we performed molecular genetic analysis on one of them, MpCLAVATA3 INSENSITIVE RECEPTOR KINASE (MpCIK). Two knockout alleles for MpCIK formed narrow apical meristems marked by promMpYUC2:GUS marker, which were not expanded by MpCLE2 peptide treatment, phenocopying Mpclv1. Loss of sensitivity to MpCLE2 peptide was also observed in gemma cup formation in both Mpclv1 and Mpcik. Biochemical analysis using a Nicotiana benthamiana transient expression system revealed weak association between MpCIK and MpCLV1, as well as MpCIK and MpTDR. While MpCIK may also participate in MpCLE1 signaling, our data show that the conserved CLV3-CLV1-CIK module functions in M. polymorpha, controlling meristem activity for development and organ formation for asexual reproduction.

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.

Sign in / Sign up

Export Citation Format

Share Document