Dramatic Change in Function and Expression Pattern of a Gene Duplicated by Polyploidy Created a Paternal Effect Gene in the Brassicaceae

Abstract

New gene formation by polyploidy has been an ongoing process during the evolution of various eukaryotes that has contributed greatly to the large number of genes in their genomes. After duplication, some genes that are retained can acquire new functions or expression patterns, or subdivide their functions or expression patterns between duplicates. Here, we show that SHORT SUSPENSOR (SSP) and Brassinosteroid Kinase 1 (BSK1) are paralogs duplicated by a polyploidy event that occurred in the Brassicaceae family about 23 Ma. SSP is involved in paternal control of zygote elongation in Arabidopsis thaliana by transcription in the sperm cells of pollen and then translation in the zygote, whereas BSK1 is involved in brassinosteroid signal transduction. Comparative analysis of expression in 63 different organs and developmental stages revealed that BSK1 and SSP have opposite expression patterns in pollen compared with all other parts of the plant. We determined that BSK1 retains the ancestral expression pattern and function. Thus, SSP has diverged in function after duplication from a component of the brassinosteroid signaling pathway to a paternal regulator of the timing of zygote elongation. The ancestral function of SSP was lost by deletions in the kinase domain. Our sequence rate analysis revealed that SSP but not BSK1 has experienced a greatly accelerated rate of amino acid sequence changes and relaxation of purifying selection. In addition, SSP has been duplicated to create a new gene (SSP-like1) with a completely different expression pattern, a shorter coding sequence that has lost a critical functional domain, and a greatly accelerated rate of amino acid sequence evolution along with evidence for positive selection, together indicative of neofunctionalization. This study illustrates two dramatic examples of neofunctionalization following gene duplication by complete changes in expression pattern and function. In addition, our findings indicate that paternal control of zygote elongation by SSP is an evolutionarily recent innovation in the Brassicaceae family.

BnaC9.SMG7b functions as a positive regulator of number of seeds per silique in rapeseed (Brassica napus L.) by regulating the formation of functional female gametophytes

“…Functional divergence of duplicated genes provides a source of evolutionary novelties in polyploids, including pseudogenization, neofunctionalization, and subfunctionalization (Force et al, 1999;Conant and Wolfe, 2008;Liu and Adams, 2010). Our study showed that an obvious subfunctionalization occurred in BnaC9.…”

Kin Conflict in Seed Development: An Interdependent but Fractious Collective

“…Similar studies in maize (Waters et al 2011) and SSP mRNAs carried by Arabidopsis sperm are translated in zygotes and regulate the first asymmetric cell division that establishes apical (embryo) and basal (suspensor) cell fates (Bayer et al 2009). SSP acquired its current function sometime after a whole-genome duplication in an ancestor of the Brassicaceae (Liu & Adams 2010). mRNAs transcribed in male gametophytes and delivered to zygotes via sperm are subject to the same selective forces as PEGs transcribed in embryos after fertilization.…”

Spatiotemporal Seed Development Analysis Provides Insight into Primary Dormancy Induction and Evolution of theLepidium DELAY OF GERMINATION1Genes

“…It is tempting to speculate that in L. papillosum, the two LepaDOG1a and LepaDOG1c proteins provide functional roles in dormancy regulation that are fulfilled by different splice variants of the single AtDOG1 gene (Bentsink et al, 2006;Nakabayashi et al, 2012) in the shrunken genome of Arabidopsis, which is characterized by extensive gene loss (Thomas et al, 2006;Oyama et al, 2008). Furthermore, polyploidization can form the basis for neofunctionalization or subfunctionalization of multiplied and retained genes (homeologs; Erdmann et al, 2010;Liu and Adams, 2010;Franzke et al, 2011), providing a mechanism for potentially diversified or more complex functions of the individual LepaDOG1 proteins in a putatively conserved dormancy mechanism. As outlined above, we propose that L. papillosum evolved by autopolyploidization or allopolyploidization from the very closely related L. oxytrichum (or its progenitor).…”