Abstract
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.
Highlights
The life cycles of eukaryotes alternate between diploid (2n ) and haploid (n) phases through meiosis and fertilization (Bowman et al, 2016)
The egg-specific expression of MpKNOX1 is in sharp contrast with the expression pattern of KNOX1 genes in another model bryophyte, P. patens, where all three KNOX1 genes are strongly expressed in sporophytes to regulate their development (Sakakibara et al, 2008)
The egg-specific expression pattern of MpKNOX1 is reminiscent of that of GSM1, a KNOX gene of the unicellular green alga C. reinhardtii expressed in minus gametes
Summary
The life cycles of eukaryotes alternate between diploid (2n ) and haploid (n) phases through meiosis and fertilization (Bowman et al, 2016). The sporophytes of extant flowering plants (angiosperms) exhibit far more complex morphologies than their male and female gametophytes, the pollen grain, and embryo sac, respectively, which are composed of only a few cells This evolutionary transition in life cycle is thought to have been facilitated by the cooption of genes and/or gene regulatory networks that regulate gametophyte development to function in sporophyte development (Bowman et al, 2019). In the fungi Saccharomyces cerevisiae and Coprinopsis cinerea, TALE and non-TALE HD TFs are expressed in haploid cells of opposite mating types (Herskowitz, 1989; Kues et al, 1992) These proteins heterodimerize in zygotes to regulate the expression of genes promoting the haloid-to-diploid transition (Goutte and Johnson, 1988; Spit et al, 1998). We uncovered inverted sex-specific expression patterns of KNOX and BELL genes between C. reinhardtii and M. polymorpha, suggesting that anisogamy evolved independently of KNOX/BELL expression in gametes
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