Evolution of Class III Homeodomain–Leucine Zipper Genes in Streptophytes

Abstract

Land plants underwent tremendous evolutionary change following the divergence of the ancestral lineage from algal relatives. Several important developmental innovations appeared as the embryophyte clade diversified, leading to the appearance of new organs and tissue types. To understand how these changes came about, we need to identify the fundamental genetic developmental programs that are responsible for growth, patterning, and differentiation and describe how these programs were modified and elaborated through time to produce novel morphologies. Class III homeodomain-leucine zipper (class III HD-Zip) genes, identified in the model plant Arabidopsis thaliana, provide good candidates for basic land plant patterning genes. We show that these genes may have evolved in a common ancestor of land plants and their algal sister group and that the gene family has diversified as land plant lineages have diversified. Phylogenetic analysis, expression data from nonflowering lineages, and evidence from Arabidopsis and other flowering plants indicate that class III HD-Zip genes acquired new functions in sporophyte apical growth, vascular patterning and differentiation, and leaf development. Modification of expression patterns that accompanied diversification of class III HD-Zip genes likely played an important role in the evolution of land plant form.

Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs

“…In addition, previous reports indicate that no miR156 or miR166 sequences could be detected in gel blots of C. corallina total RNA 23 , and the putative Chara miR165/miR166 target sequence contains five mismatches relative to the canonical miR166 sequence 5 0 -CCCC UUACUUCGGACCAGGCU-3 0 (ref. 24). All these data suggest that the early evolution of complex multicellular body plans occurred independently of conserved higher plant miRNAs.…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…The origin of two major groups of HD-ZIP proteins (class III and class IV) has been traced back to charophyte algae (Floyd et al 2006;Zalewski et al 2013). Although HD-ZIP proteins are also found in bryophytes, their function in lower plants is not well characterized (Sakakibara et al 2001;Prigge and Clark 2006).…”

“…Although HD-ZIP proteins are also found in bryophytes, their function in lower plants is not well characterized (Sakakibara et al 2001;Prigge and Clark 2006). Interestingly, a micro-RNA binding site that regulates expression of class III HD-ZIP expression in angiosperms is conserved in lower plants, but not in Chara, suggesting that gene family expansion and regulatory evolution contributed to functional novelty in embryophyte HD-ZIPs (Floyd et al 2006;Floyd and Bowman 2007). Wuschel-like homeodomain proteins that are important for Angiosperm shoot apical meristem identity are also present in charophyte algae, but their role in this group and bryophytes has not been explored (Timme and Delwiche 2010).…”

Organ Polarity in Plants Is Specified through the Opposing Activity of Two Distinct Small Regulatory RNAs

“…The miR165/166-directed cleavage of HD-ZIPIII transcripts is conserved in basal lineages of land plants, including bryophytes, lycopods, and ferns . Organ polarity is a relatively recent landmark in plant development; thus, it is possible that the regulation of HD-ZIPIII genes by miR165/166 evolved as a preadaptation that was later co-opted for use in adaxial/abaxial patterning of leaves and other lateral organs (Floyd et al 2006).…”