Evolution in the Cycles of Life

Bowman, John L.; Sakakibara, Keiko; Furumizu, Chihiro; Dierschke, Tom

doi:10.1146/annurev-genet-120215-035227

Cited by 95 publications

(90 citation statements)

References 122 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Rather, striking conservation of KNOX/BELL functions in the promotion of karyogamy across phylogenetically distant M. polymorpha and C. reinhardtii suggests that functions of KNOX/BELL heterodimers shifted from zygote-activation to sporophyte development as land plant evolved. This view is consistent with a proposed evolutionary scenario of HD proteins in a broader eukaryotic taxa, including fungi and metazoans (Bowman et al, 2016).…”

Section: Discussionsupporting

confidence: 90%

See 1 more Smart Citation

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

Hisanaga

Fujimoto

Cui

et al. 2020

Preprint

View full text Add to dashboard Cite

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...

show abstract

Section: Discussionsupporting

confidence: 90%

“…Outside the plant kingdom, TALE TFs in yeasts and fungi promote the haploid-to-diploid transition (Goutte and Johnson, 1988, Herskowitz, 1989, Kües et al, 1992, Spit et al, 1998). Thus, perhaps the shared zygote-activating functions of KNOX/BELL in M. polymorpha and C. reinhardtii reflect an ancestral state (Bowman et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

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

Hisanaga

Fujimoto

Cui

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…With the emergence of complex, multicellular organisms, it would not have been surprising if additional processes such as developmental networks had come under the control of these regulators as this would have ensured that those developmental processes were deployed at the appropriate stage of the life cycle . Indeed, it has been suggested that modifications to homeodomain-based regulatory circuits may have played an important role in the emergence of sporophyte complexity in the green lineage (Bowman et al, 2016;Lee et al, 2008). Key events may have included the replacement of the Gsp1-like class of BELL-related1 genes with alternative (true BEL-class) proteins and diversification of both the true BELL-class and the KNOX-class TALE HD TFs.…”

Section: Discussionmentioning

confidence: 99%

Convergent recruitment of life cycle regulators to direct sporophyte development in two eukaryotic supergroups

Arun

Af³

et al. 2018

Preprint

View full text Add to dashboard Cite

Three amino acid loop extension homeodomain transcription factors (TALE HD TFs) act as life cycle regulators in green algae and land plants. In mosses these regulators are required for the deployment of the sporophyte developmental program. We demonstrate that mutations in either of two TALE HD TF genes, OUROBOROS or SAMSARA, in the brown alga Ectocarpus result in conversion of the sporophyte generation into a gametophyte. The OUROBOROS and SAMSARA proteins heterodimerise in a similar manner to TALE HD TF life cycle regulators in the green lineage. These observations demonstrate that TALE-HD-TFbased life cycle regulation systems have an extremely ancient origin, and that these systems have been independently recruited to regulate sporophyte developmental programs in at least two different complex multicellular eukaryotic supergroups, Archaeplastida and Chromalveolata.

show abstract

“…Furthermore, despite the extensive literature on the functions of KNOX/BELL in angiosperms, the only potential known vestige of this ancestral system existing in angiosperms is the presence of KNOX2 function in the Arabidopsis female gametophyte, possibly in the egg cell (Pagnussat et al, 2007). Thus, it seems that the ancestral function has been entirely lost in some derived land plants, as it has presumably in the metazoan lineage (Bowman et al, 2016b). (Marchant, 1713, Mirbel, 1835, Thuret, 1851, Unger, 1837.…”

Section: An Ancestral Function For Tale-hd Genes In the Viridiplantaementioning

confidence: 99%

“…Expression of paralogous homeodomain genes in the two gametes directs the haploid-to-diploid transition in gene expression in phylogenetically diverse eukaryotes, including the ascomycete fungus Saccharomyces cerevisiae (Goutte andJohnson, 1988, Herskowitz, 1989), the basidiomycete fungi Coprinopsis cinerea and Ustilago maydis (Gillissen et al, 1992, Hull et al, 2005, Kues et al, 1992, Spit et al, 1998, Urban et al, 1996, the Amoebozoa Dictyostelium discoideum (Hedgethorne et al, 2017), the brown alga Ectocarpus (Arun et al, 2019), the red alga Pyropia yezoensis (Mikami et al, 2019), and the unicellular Chlorophyte alga Chlamydomonas reinhardtii (Ferris and Goodenough, 1987, Lee et al, 2008, Nishimura et al, 2012, Zhao et al, 2001. This broad phylogenetic distribution suggest this was an ancestral function of homeodomain genes [reviewed in (Bowman et al, 2016b)]. In the Viridiplantae the paralogous genes are two subclasses, KNOX and BELL, of TALE-class homeodomain (HD) genes.…”

Section: Main Text: Introductionmentioning

confidence: 99%

Gamete-specific expression of TALE class HD genes activates the diploid sporophyte program inMarchantia polymorpha

Dierschke

Flores-Sondoval

Rast-Somssich

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Eukaryotic life cycles alternate between haploid and diploid phases and in phylogenetically diverse unicellular eukaryotes, expression of paralogous homeodomain genes in the two gametes directs the haploid-to-diploid transition. In the unicellular Chlorophyte alga Chlamydomonas KNOX and BELL TALE-homeodomain genes mediate the transition. Here we demonstrate that in the liverwort Marchantia polymorpha paternal (sperm) expression three of the five phylogenetically diverse BELL genes, MpBELL234, and maternal (egg) expression of MpKNOX1 mediate the haploid-to-diploid transition. Loss-of-function alleles of either result in zygotic or early embryonic arrest. In land plants both the haploid gametophyte and diploid sporophyte are complex multicellular organisms. Expression of MpKNOX1 and two other paralogs, MpBELL1 and MpKNOX2, during sporophyte development is consistent with a later role in patterning the sporophyte. These results indicate that the ancestral mechanism to activate diploid gene expression was retained in early diverging land plants and subsequently co-opted during evolution of the diploid sporophyte body.

show abstract

Evolution in the Cycles of Life

Cited by 95 publications

References 122 publications

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

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

Convergent recruitment of life cycle regulators to direct sporophyte development in two eukaryotic supergroups

Gamete-specific expression of TALE class HD genes activates the diploid sporophyte program inMarchantia polymorpha

Contact Info

Product

Resources

About