Divergent evolutionary fates of major photosynthetic gene networks following gene and whole genome duplications

Abstract

Gene and genome duplication are recurring processes in flowering plants, and elucidating the mechanisms by which duplicated genes are lost or deployed is a key component of understanding plant evolution. Using gene ontologies (GO) or protein family (PFAM) domains, distinct patterns of duplicate retention and loss have been identified depending on gene functional properties and duplication mechanism, but little is known about how gene networks encoding interacting proteins (protein complexes or signaling cascades) evolve in response to duplication. We examined patterns of duplicate retention within four major gene networks involved in photosynthesis (the Calvin cycle, photosystem I, photosystem II, and the light harvesting complex) across three species and four whole genome duplications, as well as small-scale duplications, and showed that photosystem gene family evolution is governed largely by dosage sensitivity. ( 1) In contrast, Calvin cycle gene families are not dosage sensitive, but exhibit a greater capacity for functional differentiation. Here we review these findings, highlight how this study, by analyzing defined gene networks, is complementary to global studies using functional annotations such as GO and PFAM, and elaborate on one example of functional differentiation in the Calvin cycle gene family, transketolase.

Figure 1

Expression levels of Arabidopsis transketolase (TKL) homeologs (AT2G45290 and AT3G60750) plotted against (A) each other and (B) against the Calvin cycle-specific genes, rubisco small subunit (RbcS), sedoheptulose-1,7-bisphosphatase (SBPase) and phoshoribulokinase (PRK), across all microarray experiments in AffyWatch release 2.0 (obtained using CressExpress23). The microarray probe for RbcS (264474_s_at) hybridizes to all four RbcS copies in Arabidopsis (AT1G67090, AT5G38410, AT5G38420, AT5G38430). SBPase = AT3G55800; PRK = AT1G32060.