Evolutionary divergence of the sex-determining gene <i>MID</i> uncoupled from the transition to anisogamy in volvocine algae

Shimin, Geng; Miyagi, Ayano; Umen, James G.

doi:10.1242/dev.162537

Cited by 15 publications

(22 citation statements)

References 74 publications

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“…Interestingly, however, the sex-specific expression patterns of KNOX and BELL in C. reinhardtii are opposite to those in M. polymorpha . In C. reinhardtii , KNOX (GSM1) and BELL (GSP1) are expressed in isogamous minus and plus gametes ( Lee et al, 2008 ), which directly evolved into male and female gametes, respectively, in oogamous (with small motile gametes and large immotile gametes) Volvox carteri, primarily by modifying genes acting downstream of the conserved sex-determinant protein MID ( Ferris and Goodenough, 1997 ; Geng et al, 2014 ; Geng et al, 2018 ; Nozaki et al, 2006 ; Figure 7B ). Results from other research groups indicate that the expression specificity of KNOX/BELL is conserved along the volvocine lineage (with minus and male gametes expressing GSM1, and plus and female gametes expressing GSP1; personal communication with Takashi Hamaji [Kyoto University, Japan] and James Umen [Donald Danforth Plant Science Center, MO]).…”

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. 2021

eLife

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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.

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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. 2021

eLife

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“…Interestingly, however, the sex-specific expression patterns of KNOX and BELL in C. reinhardtii are opposite to those in M. polymorpha . In C. reinhardtii , KNOX (GSM1) and BELL (GSP1) are expressed in isogamous minus and plus gametes (Lee et al, 2008), which directly evolved into male and female gametes, respectively, in oogamous (with small motile gametes and large immotile gametes) Volvox carteri, primarily by modifying genes acting downstream of the conserved sex-determinant protein MID (Ferris and Goodenough, 1997, Geng et al, 2014, Geng et al, 2018, Nozaki et al, 2006) (Figure 7B). Results from other research groups indicate that the expression specificity of KNOX/BELL is conserved along the volvocine lineage (with minus and male gametes expressing GSM1; personal communication with Takashi Hamaji (Kyoto University, Japan) and James Umen (Donald Danforth Plant Science Center, MO)).…”

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

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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...

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“…This requirement, in turn, suggests an evolutionary scenario from homothallic to heterothallic sex-determination wherein MID acquires plus suppression functions on top of its ancestral function of minus activation. Evolution of MID functions from its ancestral role has been also noted in a sexually dimorphic oogamous species, Volvox carteri (Geng et al 2014(Geng et al , 2018.…”

Section: Matingmentioning

confidence: 91%

Novel approaches for generating and manipulating diploid strains of Chlamydomonas reinhardtii

Kariyawasam¹,

Joo²,

Goodenough³

et al. 2019

ALGAE

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Genetic study of haploid organisms offers the advantage that mutant phenotypes are directly displayed, but has the disadvantage that strains carrying lethal mutations are not readily maintained. We describe an approach for generating and performing genetic analysis of diploid strains of Chlamydomonas reinhardtii, which is normally haploid. First protocol utilizes self-mating diploid strains that will facilitate the genetic analysis of recessive lethal mutations by offering a convenient way to produce homozygous diploids in a single mating. Second protocol is designed to reduce the chance of contamination and the accumulation of spontaneous mutations for long-term storage of mutant strains. Third protocol for inducing the meiotic program is also included to produce haploid mutant strains following tetraploid genetic analysis. We discuss implication of self-fertile strains for the future of Chlamydomonas research.

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Evolutionary divergence of the sex-determining gene MID uncoupled from the transition to anisogamy in volvocine algae

Cited by 15 publications

References 74 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

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

Novel approaches for generating and manipulating diploid strains of Chlamydomonas reinhardtii

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