In contrast to animals, in which the germ cell lineage is established during embryogenesis, plant germ cells are generated in reproductive organs via reprogramming of somatic cells. The factors that control germ cell differentiation and reprogramming in plants are poorly understood. Members of the RKD subfamily of plant-specific RWP-RK transcription factors have been implicated in egg cell formation in Arabidopsis based on their expression patterns and ability to cause an egg-like transcriptome upon ectopic expression [1]; however, genetic evidence of their involvement is lacking, due to possible genetic redundancy, haploid lethality, and the technical difficulty of analyzing egg cell differentiation in angiosperms. Here we analyzed the factors that govern germ cell formation in the liverwort Marchantia polymorpha. This recently revived model bryophyte has several characteristics that make it ideal for studies of germ cell formation, such as low levels of genetic redundancy, readily accessible germ cells, and the ability to propagate asexually via gemma formation [2, 3]. Our analyses revealed that MpRKD, a single RWP-RK factor closely related to angiosperm RKDs, is preferentially expressed in developing eggs and sperm precursors in M. polymorpha. Targeted disruption of MpRKD had no effect on the gross morphology of the vegetative and reproductive organs but led to striking defects in egg and sperm cell differentiation, demonstrating that MpRKD is an essential regulator of germ cell differentiation. Together with previous findings [1, 4-6], our results suggest that RKD factors are evolutionarily conserved regulators of germ cell differentiation in land plants.
Plant life cycles alternate between haploid gametophytes and diploid sporophytes. While regulatory factors determining male and female sexual morphologies have been identified for sporophytic reproductive organs, such as stamens and pistils of angiosperms, those regulating sex‐specific traits in the haploid gametophytes that produce male and female gametes and hence are central to plant sexual reproduction are poorly understood. Here, we identified a MYB‐type transcription factor, MpFGMYB, as a key regulator of female sexual differentiation in the haploid‐dominant dioicous liverwort, Marchantia polymorpha. MpFGMYB is specifically expressed in females and its loss resulted in female‐to‐male sex conversion. Strikingly, MpFGMYB expression is suppressed in males by a cis‐acting antisense gene SUF at the same locus, and loss‐of‐function suf mutations resulted in male‐to‐female sex conversion. Thus, the bidirectional transcription module at the MpFGMYB/SUF locus acts as a toggle between female and male sexual differentiation in M. polymorpha gametophytes. Arabidopsis thaliana MpFGMYB orthologs are known to be expressed in embryo sacs and promote their development. Thus, phylogenetically related MYB transcription factors regulate female gametophyte development across land plants.
Leaves are ideal model systems to study the organ size regulation of multicellular plants. Leaf cell number and cell size are determinant factors of leaf size which is controlled through cell proliferation and post-mitotic cell expansion, respectively. To achieve a proper leaf size, cell proliferation and post-mitotic cell expansion should be co-ordinated during leaf morphogenesis. Compensation, which is enhanced post-mitotic cell expansion associated with a decrease in cell number during lateral organ development, is suggestive of such co-ordination. Genetic and kinematic studies revealed at least three classes of modes of compensation, indicating that compensation is a heterogeneous phenomenon. Recent studies have increased our understanding about the molecular basis of compensation by identifying the causal genes of each compensation-exhibiting mutant. Furthermore, analyses using chimeric leaves revealed that a type of compensated cell expansion requires cell-to-cell communication. Information from recent advances in molecular and genetic studies on compensation has been integrated here and its role in organ size regulation is discussed.
During leaf development, a decrease in cell number often triggers an increase in cell size. This phenomenon, called compensation, suggests that some system coordinates cell proliferation and cell expansion, but how this is mediated at the molecular level is still unclear. The fugu2 mutants in Arabidopsis (Arabidopsis thaliana) exhibit typical compensation phenotypes. Here, we report that the FUGU2 gene encodes FASCIATA1 (FAS1), the p150 subunit of Chromatin Assembly Factor1. To uncover how the fas1 mutation induces compensation, we performed microarray analyses and found that many genes involved in the DNA damage response are up-regulated in fas1. Our genetic analysis further showed that activation of the DNA damage response and the accompanying decrease of cell number in fas1 depend on ATAXIA TELANGIECTASIA MUTATED (ATM) but not on ATM AND RAD3 RELATED. Kinematic analysis suggested that the delay in the cell cycle leads to a decrease in cell number in fas1 and that loss of ATM partially restores this phenotype. Consistently, both cell size phenotypes and high ploidy phenotypes of fas1 are also suppressed by atm, supporting that the ATM-dependent DNA damage response leads to these phenotypes. Altogether, these data suggest that the ATM-dependent DNA damage response acts as an upstream trigger in fas1 to delay the cell cycle and promote entry into the endocycle, resulting in compensated cell expansion.
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.
20 21 KNOX and BELL transcription factors regulate distinct steps of diploid development in 22 the green lineages. In the green alga Chlamydomonas reinhardtii, KNOX and BELL 23 proteins are inherited by gametes of the opposite mating types, and heterodimerize in 24 zygotes to activate diploid development. By contrast, in land plants such as 25 Physcomitrella and Arabidopsis, KNOX and BELL proteins function in meristem 26 maintenance and organogenesis during the later stages of diploid development. However, 27 whether the contrasting functions of KNOX and BELL were acquired independently in 28 algae and land plants is currently unknown. Here we show that in the basal land plant 29 species Marchantia polymorpha, gamete-expressed KNOX and BELL are required to 30 initiate zygotic development by promoting nuclear fusion in a manner strikingly similar 31 to that of C. reinhardtii. Our results indicate that zygote activation is the ancestral role of 32 KNOX/BELL transcription factors, which shifted toward meristem maintenance as land 33 plants evolved. 34 35 106 6 the functional transition of KNOX/BELL from zygote activation to sporophyte 107 morphogenesis occurred at least once in the land plant lineage independently of the 108 acquisition of multicellular sporophytes. Additionally, we uncovered inverted sex-109 specific expression patterns of KNOX and BELL genes between C. reinhardtii and M. 110 polymorpha, suggesting that anisogamy evolved independently of KNOX/BELL 111 expression in gametes.112 113 Results 114MpKNOX1 is as an egg-specific gene in M. polymorpha 115 We previously reported that an RWP-RK TF MpRKD promotes egg cell differentiation 116 in M. polymorpha. Loss-of-function Mprkd mutant females grow normally and produce 117 archegonia like the wild type, but their egg cells do not mature, instead degenerating after 118 ectopic cell division and vacuolization (Koi et al., 2016). We made use of this egg-specific 119 defect in Mprkd to identify genes preferentially expressed in egg cells of M. polymorpha. 120 Briefly, we collected ~2,000 archegonia from two independent Mprkd female mutant 121 lines (Mprkd-1 and Mprkd-3, Koi et al., 2016), each in two replicates. As a control, 122 ~4,000 archegonia were collected from wild-type females in four replicates. We extracted 123 RNA from each pool and analyzed it by next-generation sequencing. Comparative 124 transcriptome analysis identified 1,583 genes with significantly reduced mRNA levels in 125 Mprkd compared to wild-type archegonia (>3-fold and false discovery rate < 0.01; Figure 126 1A and Figure1 -figure supplement 1A). Among these, MpKNOX1 (Mp5g01600), the 127 only class I KNOX gene in M. polymorpha (Bowman et al., 2017, Frangedakis et al., 128 2017), was strongly downregulated in Mprkd vs. the wild type (~500-fold) (Figure 1B). 129 7 The MpKNOX1 polypeptide contains KNOX I, KNOX II, ELK, and Homeobox domains, 130as do KNOX proteins from green algae, mosses, ferns and flowering plants ( Figure 1C). 131Previous RNA-sequencing data (Bowman et al., 2017) indi...
Complex mechanisms regulate gene dosage throughout eukaryotic life cycles. Mechanisms controlling gene dosage have been extensively studied in animals, however it is unknown how generalizable these mechanisms are to diverse eukaryotes. Here, we use the haploid plant Marchantia polymorpha to assess gene dosage control in its short-lived diploid embryo. We show that throughout embryogenesis, paternal chromosomes are repressed resulting in functional haploidy. The paternal genome is targeted for genomic imprinting by the Polycomb mark H3K27me3 starting at fertilization, rendering the maternal genome in control of embryogenesis. Maintaining haploid gene dosage by this new form of imprinting is essential for embryonic development. Our findings illustrate how haploid-dominant species can regulate gene dosage through paternal chromosome inactivation and initiates the exploration of the link between life cycle history and gene dosage in a broader range of organisms.
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