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

Abstract

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.

Molecular mechanisms involved in functional macroevolution of plant transcription factors

“…Studies have addressed the coevolutionary history of the TALE homeodomain KNOX/ BELL TF complex. Their ability to heterodimerize and migrate to the nucleus is conserved in land plants and algae (Bowman et al ., 2016; Horst et al ., 2016; Dierschke et al ., 2020). The KNOX‐BELL heterodimerization is required to initiate the diploid programme in Chlamydomonas zygotes (Lee et al ., 2008).…”

“…On the other hand, Class I KNOX ( KNOX1 ) are expressed and participate in sporophyte development but not in the gametophytic meristem in bryophytes and ferns (Sakakibara et al ., 2008; Dierschke et al ., 2020; Hisanaga, 2020), suggesting it was not co‐opted as other regulators (see below). Also, the overexpression of fern or Physcomitrella versions in Arabidopsis resembles the AtKNOX1 overexpression leaf serration phenotype (Sakakibara et al ., 2008) and Pp MKN2 can phenotypically complement the Arabidopsis brevipedicellus mutant defect in silique‐insertion angle, but KNOX1 homologues from vascular plants cannot complement the Physcomitrella mkn2/4/5 triple mutant defect in sporophyte development (Frangedakis et al ., 2017).…”

The epigenetic origin of life history transitions in plants and algae

“…Among H3K27me3-silenced genes in bryophytes are the evolutionary conserved BELL and KNOX TALEhomeodomain transcription factors (TF), which interact to activate diploid gene expression and zygote formation in Chlamydomonas and Marchantia (Lee et al 2008;Widiez et al 2014;Horst and Reski 2016;Dierschke et al 2020). Interestingly, ectopic overexpression of BELL1 in Physcomitrella induces embryo and sporophyte formation in the absence of fertilization .…”

“…PRC2 still functions today to repress TE activity in unicellular red and green algae (Mikulski et al 2017) but also bryophytes (Montgomery et al 2020). At some point in the evolution of early land plants, PRC2 began to silence gene expression, which included the BELL/KNOX system that regulates the diploid program in green algae and bryophytes (Lee et al 2008;Widiez et al 2014;Horst and Reski 2016;Dierschke et al 2020). This scenario would have led to repression of the sporophyte program and extension of the gametophytic phase, which is still evident in modern-day bryophytes.…”

The hornworts: morphology, evolution and development

“…In M . polymorpha a class 1 KNOX protein is expressed in the egg and is necessary for the formation of the zygote via interaction with two paternally inherited BELL proteins (Mp BELL3 and/or Mp BELL4 ) (Dierschke et al ., 2020), a function similar to the KNOX function in C . reinhardtii .…”