Divergence of duplicated genes by repeated partitioning of splice forms and subcellular localization

Abstract

Summary Gene duplication is a prominent and recurrent process in plant genomes. Among the possible fates of duplicated genes, subfunctionalization refers to duplicates taking on different parts of the function or expression pattern of the ancestral gene. This partitioning could be accompanied by changes in subcellular localization of the protein products. When alternative splicing of gene products leads to protein products with different subcellular localizations, we propose that after gene duplication there will be partitioning of the alternatively spliced forms such that the products of each duplicate are localized to only one of the original locations, which we refer to as sublocalization. We identified the plastid ascorbate peroxidase (cpAPX) genes across angiosperms and analyzed their duplication history, alternative splicing, and subcellular targeting patterns to identify cases of sublocalization. We found angiosperms typically have one cpAPX gene that generates both thylakoidal APX (tAPX) and stromal APX (sAPX) through alternative splicing. We identified several independent lineage‐specific sublocalization cases with specialized paralogues of tAPX and sAPX. We determined that the sublocalization happened through two types of sequence evolution patterns. Our findings suggest that the divergence through sublocalization is key to the retention of paralogous cpAPX genes in angiosperms.

The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible

“…Of course, whether or not subgenome conflicts exist may be partly a question of the preexisting differences between the parental species, and a more general survey of allopolyploidies that includes estimates of the subgenome divergence prior to the polyploidy events would be most enlightening. If the pattern holds, however, the implications could be significant: hybridization represents a potentially important means of adaption (Paterson 2005;Hollister 2015;Alix et al 2017;Blanc-Mathieu et al 2017;Smukowski Heil et al 2017), and if we combine this factor with the propensity for polyploidies to generate evolutionary innovations (Edger et al 2015) and the value of holding dosage sensitive genes in duplicate long enough to allow such innovations (Blanc and Wolfe 2004;Conant and Wolfe 2008b;Conant et al 2014;Zhao et al 2017;Liang and Schnable 2018;Qiu et al 2020), we can find ourselves in a position to strongly support Ohno's arguments on the power of polyploidy.…”

Generating and characterizing single- and multigene mutants of the Rubisco small subunit family in Arabidopsis

“…As a product of gene duplication, 1B is subject to selection pressure and is not retained in all accessions of Arabidopsis, although loss was correlated with disruption of the promoter (Schwarte and Tiedemann, 2011). Retention of 1B may be linked to sublocalization (Qiu et al, 2019). Differential expression patterns of rbcS genes in different organs have also been observed in other plant species including tomato, maize, tobacco, and rice (Wanner and Gruissem, 1991;Ewing et al, 1998;Morita, et al, 2014;Laterre et al, 2017).…”

Expression Partitioning of Duplicate Genes at Single Cell Resolution in Arabidopsis Roots

“…Single cell tools already exist for addressing these issues by assaying chromatin accessibility ( Farmer et al, 2020 ) and mapping the epigenomic landscape of the cell ( Zhou et al, 2019 ). For understanding functional differences between paralogs, and for even finer scale “sub-localization” of gene action within cells that may be a driver of paralog retention ( Qiu et al, 2019 ), a host of other single cell-omics tools exist or are under development ( Macaulay et al, 2017 ; Hasle et al, 2020 ).…”