Gamete expression of TALE class HD genes activates the diploid sporophyte program in <i>Marchantia polymorpha</i>.

Abstract

Eukaryotic life cycles alternate between haploid and diploid phases and in phylogenetically diverse unicellular eukaryotes, expression of paralogous homeodomain genes in gametes primes the haploid-to-diploid transition. In the unicellular chlorophyte alga <i>Chlamydomonas,</i> KNOX and BELL TALE-homeodomain genes mediate this transition. We demonstrate that in the liverwort <i>Marchantia polymorpha,</i> paternal (sperm) expression of three of five phylogenetically diverse BELL genes, Mp<i>BELL234</i>, and maternal (egg) expression of both Mp<i>KNOX1</i> and Mp<i>BELL34</i> mediate the haploid-to-diploid transition. Loss-of-function alleles of Mp<i>KNOX1</i> result in zygotic arrest, whereas a loss of either maternal or paternal Mp<i>BELL234</i> results in variable zygotic and early embryonic arrest. Expression of Mp<i>KNOX1</i> and Mp<i>BELL34</i> during diploid sporophyte development is consistent with a later role for these genes 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.