Academic journal article Genetics

Evolution of Class III Homeodomain-Leucine Zipper Genes in Streptophytes

Academic journal article Genetics

Evolution of Class III Homeodomain-Leucine Zipper Genes in Streptophytes

Article excerpt

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.

LAND plants (embryophytes) compose a monophyletic group that together with the charophycean green algae form the streptophyte clade (MISHLER et al. 1994; KENRICK and CRANE 1997; BHATTACHARYA et al. 1998). Recent molecular phylogenetic analyses resolve the charophycean group Charales as sister to land plants (KAROL et al. 2001; DELWICHE et al. 2002) (Figure 1). These phylogenetic analyses along with comparative analysis of ultrastructure and biochemistry indicate that land plants evolved from a freshwater charophycean green algal ancestor and that ancestor possessed certain developmental features that were inherited by land plants and are shared with extant charophytes (GRAHAM 1993; GRAHAM et al. 2000; COOK 2004).

However, the origin and diversification of embryophytes from algal ancestors also involved dramatic evolutionary changes. Several innovations allowed for the diversification of the relatively simple and diminutive ancestral land plant into a lineage of increasingly complex and diverse forms and life histories. These evolutionary innovations included the origin of the diploid sporophyte (embryo), histogenesis directly from an apical meristem, apical growth and branching in the sporophyte generation, the origin of lignified conducting and support tissues, the origin of roots, and the origin of leaves (Figure 1) (GRAHAM et al. 2000; NIKLAS 2000; SUSSEX and KERK 2001; BOYCE and KNOLL 2002; COOKE et al. 2002; FRIEDMAN et al. 2004). It has also been proposed that evolutionary changes in auxin action were essential for increasing complexity of land plant form (COOKE et al. 2002).

The key to understanding morphological evolution in multicellular organisms is determining fundamental components of the developmental patterning systems that have been modified through time to produce novel body plans (CARROLL 2000). To learn how evolutionary changes in development have played a role in producing morphological diversity and complexity in plants, it is essential to understand the genetic basis of developmental evolution (GRAHAM et al. 2000; NIKLAS 2000; SUSSEX and KERK 2001; BOYCE and KNOLL 2002; COOKE et al. 2002; FRIEDMAN et al. 2004). We must look to model genetic systems and focus on developmental genes that are known to play a fundamental role in the establishment of growth and patterning throughout the plant body and throughout the life of a plant. Genes such as these would provide likely candidates for part of a developmental tool kit that has been modified through time to allow the origin of the new tissues and organs that have characterized land plant evolution. …

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