Abstract
The sexual cycle of the unicellular Chlamydomonas reinhardtii culminates in the formation of diploid zygotes that differentiate into dormant spores that eventually undergo meiosis. Mating between gametes induces rapid cell wall shedding via the enzyme g-lysin; cell fusion is followed by heterodimerization of sex-specific homeobox transcription factors, GSM1 and GSP1, and initiation of zygote-specific gene expression. To investigate the genetic underpinnings of the zygote developmental pathway, we performed comparative transcriptome analysis of both pre- and post-fertilization samples. We identified 253 transcripts specifically enriched in early zygotes, 82% of which were not up-regulated in gsp1 null zygotes. We also found that the GSM1/GSP1 heterodimer negatively regulates the vegetative wall program at the posttranscriptional level, enabling prompt transition from vegetative wall to zygotic wall assembly. Annotation of the g-lysin-induced and early zygote genes reveals distinct vegetative and zygotic wall programs, supported by concerted up-regulation of genes encoding cell wall-modifying enzymes and proteins involved in nucleotide-sugar metabolism. The haploid-to-diploid transition in Chlamydomonas is masterfully controlled by the GSM1/GSP1 heterodimer, translating fertilization and gamete coalescence into a bona fide differentiation program. The fertilization-triggered integration of genes required to make related, but structurally and functionally distinct organelles-the vegetative versus zygote cell wall-presents a likely scenario for the evolution of complex developmental gene regulatory networks.
Highlights
72 Metazoa, Embryophyta, and Fungi, the so-called called crown groups, independently evolved developmental programs that give rise to complex multicellular organisms
The FUS1 gene, exclusive to MTL+, encodes a glycoprotein required for the plus gametes to bind and fuse to minus gametes (Ferris et al 1996), and the MID gene, exclusive to MTL, encodes a transcription factor in the RWP-RK family that induces the minus sex program and suppresses the plus sex program (Lin and Goodenough 2007; Ferris and Goodenough 1997). Both MTL+ and MTL- are necessary for a successful progression through the sexual cycle. 138 Minus and plus sexual programs employ a series of key players acting in pairs that are expressed in a sex-specific manner: agglutinins (SAD1 and SAG1) on the flagellar membrane (Ferris et al 2005; Goodenough et al 1985), fusion[141] enabling factors (HAP2 and FUS1) on the plasma membrane (Misamore et al 142 2003; Liu et al 2015; 2008), and heterodimeric transcription factors in the
Of the remaining 46 EZ-core genes showing no significant up-regulation in 348 bp31C zygotes, 34 genes are either poorly expressed in bp31C zygotes or found to be g-lysin-inducible, meaning that most (207/219, 94.5%) of the EZ-core genes are dependent on GSP1 for EZ-expression. 352 We examined the differential expression of EZ-core in the pseudozygotes (PZ condition) where the zygote program is activated by ectopic expression of GSM1/GSP1 without gamete fusion
Summary
72 Metazoa, Embryophyta, and Fungi, the so-called called crown groups, independently evolved developmental programs that give rise to complex multicellular organisms. The Chlamydomonas heterodimeric transcription factors GSM1/GSP1 in the zygote are structural and functional homologs to the KNOX/BELL homeobox heterodimers that are involved in the diploid development of land plants (Sakakibara et al 2008; 2013; Horst et al, 2015) Such deeply rooted conservation of sexual GRNs suggests their fundamental importance for complex multicellular evolution. Zygote development entails signature events largely completed within the first 12 167 hr, such as zygote-specific wall assembly (Minami and Goodenough 1978; Woessner and Goodenough 1989; Suzuki et al 2000), selective destruction of chloroplast nucleoids derived from minus gametes and of mitochondrial DNAs from plus gametes (Kuroiwa et al 1982; Aoyama et al 2006), flagellar resorption and basal-body disassembly (Cavalier-Smith 1974; Pan and Snell 2005), and nuclear and chloroplastic fusion (Cavalier-Smith 1976) Such a rapid differentiation process would require robust regulatory networks to prevent promiscuous execution, networks that combine intra- and perhaps intercellular cues and coordinate a multitude of events. Our results define the predominant role of the GSM1/GSP1 heterodimer, and provide molecular insights concerning how various cellular machineries participate in zygote differentiation. 224
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