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 ◽  
...  

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.

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.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Suvi Honkanen ◽  
Anna Thamm ◽  
Mario A Arteaga-Vazquez ◽  
Liam Dolan

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.


2018 ◽  
Vol 120 ◽  
pp. S116
Author(s):  
Ana Maria Cunha ◽  
Sara Laranjeira ◽  
Shweta Singh ◽  
João Raimundo ◽  
Rómulo Sobral ◽  
...  

2006 ◽  
Vol 4 (4) ◽  
pp. 3-9
Author(s):  
Maria A Osipova ◽  
Elena A Dolgikh ◽  
Ludmila A Lutova

Homeodomain-containing transcription factors are the important regulators of multicellular organism's development. Plant transcription factors WOX and KNOX play the key role in meristem maintenance, controlling cell proliferation and preventing differentiation. The precise mechanism of WOX and KNOX action hasn't been well studied, however these transcription factors were shown to play the important role in plant hormones homeostasis, cytokinins in particular. Plant transcription factors of KNOX group demonstrate the similarities in structure and are supposed have the common origin with animal transcription factors of MEIS group. This review describes WOX and KNOX transcription factor families, their interaction with plant hormones. The role of homeodomain-containing transcription factors in plant and animal tumor formation is discussed.


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.


Cell Research ◽  
2008 ◽  
Vol 18 (7) ◽  
pp. 756-767 ◽  
Author(s):  
Qingyun Bu ◽  
Hongling Jiang ◽  
Chang-Bao Li ◽  
Qingzhe Zhai ◽  
Jie Zhang ◽  
...  

2021 ◽  
Vol 23 (1) ◽  
pp. 158
Author(s):  
Li Zhang ◽  
Tianhong Li ◽  
Shengzhong Su ◽  
Hao Peng ◽  
Sudi Li ◽  
...  

COP1/SPA1 complex in Arabidopsis inhibits photomorphogenesis through the ubiquitination of multiple photo-responsive transcription factors in darkness, but such inhibiting function of COP1/SPA1 complex would be suppressed by cryptochromes in blue light. Extensive studies have been conducted on these mechanisms in Arabidopsis whereas little attention has been focused on whether another branch of land plants bryophyte utilizes this blue-light regulatory pathway. To study this problem, we conducted a study in the liverwort Marchantia polymorpha and obtained a MpSPA knock-out mutant, in which Mpspa exhibits the phenotype of an increased percentage of individuals with asymmetrical thallus growth, similar to MpCRY knock-out mutant. We also verified interactions of MpSPA with MpCRY (in a blue light-independent way) and with MpCOP1. Concomitantly, both MpSPA and MpCOP1 could interact with MpHY5, and MpSPA can promote MpCOP1 to ubiquitinate MpHY5 but MpCRY does not regulate the ubiquitination of MpHY5 by MpCOP1/MpSPA complex. These data suggest that COP1/SPA ubiquitinating HY5 is conserved in Marchantia polymorpha, but dissimilar to CRY in Arabidopsis, MpCRY is not an inhibitor of this process under blue light.


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e4051 ◽  
Author(s):  
Shixiang Yao ◽  
Lili Deng ◽  
Kaifang Zeng

Membrane-bound transcription factors (MTFs) are located in cellular membranes due to their transmembrane domains. In plants, proteolytic processing is considered to be the main mechanism for MTF activation, which ensures the liberation of MTFs from membranes and further their translocation into the nucleus to regulate gene expression; this process skips both the transcriptional and translational stages, and thus it guarantees the prompt responses of plants to various stimuli. Currently, information concerning plant MTFs is limited to model organisms, including Arabidopsis thaliana and Oryza sativa, and little is known in other plant species at the genome level. In the present study, seven membrane topology predictors widely used by the research community were employed to establish a reliable workflow for MTF identification. Genome-wide in silico analysis of MTFs was then performed in 14 plant species spanning the chlorophytes, bryophytes, gymnosperms, monocots and eudicots. A total of 1,089 MTFs have been identified from a total of 25,850 transcription factors in these 14 plant species. These MTFs belong to 52 gene family, and the top six most abundant families are the NAC (128), SBP (77), C2H2 (70), bZIP (67), MYB-related (65) and bHLH (63) families. The MTFs have transmembrane spans ranging from one to thirteen, and 71.5% and 21.1% of the MTFs have one and two transmembrane motifs, respectively. Most of the MTFs in this study have transmembrane motifs located in either N- or C-terminal regions, indicating that proteolytic cleavage could be a conserved mechanism for MTF activation. Additionally, approximately half of the MTFs in the genome of either Arabidopsis thaliana or Gossypium raimondii could be potentially regulated by alternative splicing, indicating that alternative splicing is another conserved activation mechanism for MTFs. The present study performed systematic analyses of MTFs in plant lineages at the genome level, and provides invaluable information for the research community.


2018 ◽  
Vol 115 (16) ◽  
pp. E3846-E3855 ◽  
Author(s):  
Philip Carella ◽  
Anna Gogleva ◽  
Marta Tomaselli ◽  
Carolin Alfs ◽  
Sebastian Schornack

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.


2019 ◽  
Vol 61 (3) ◽  
pp. 470-480
Author(s):  
Mai Kanazawa ◽  
Yoko Ikeda ◽  
Ryuichi Nishihama ◽  
Shohei Yamaoka ◽  
Nam-Hee Lee ◽  
...  

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.


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