Comparative Evolution of Photosynthetic Genes in Response to Polyploid and Nonpolyploid Duplication      

Abstract

The likelihood of duplicate gene retention following polyploidy varies by functional properties (e.g. gene ontologies or protein family domains), but little is known about the effects of whole-genome duplication on gene networks related by a common physiological process. Here, we examined the effects of both polyploid and nonpolyploid duplications on genes encoding the major functional groups of photosynthesis (photosystem I, photosystem II, the light-harvesting complex, and the Calvin cycle) in the cultivated soybean (Glycine max), which has experienced two rounds of whole-genome duplication. Photosystem gene families exhibit retention patterns consistent with dosage sensitivity (preferential retention of polyploid duplicates and elimination of nonpolyploid duplicates), whereas Calvin cycle and light-harvesting complex gene families do not. We observed similar patterns in barrel medic (Medicago truncatula), which shared the older genome duplication with soybean but has evolved independently for approximately 50 million years, and in Arabidopsis (Arabidopsis thaliana), which experienced two nested polyploidy events independent from the legume duplications. In both soybean and Arabidopsis, Calvin cycle gene duplicates exhibit a greater capacity for functional differentiation than do duplicates within the photosystems, which likely explains the greater retention of ancient, nonpolyploid duplicates and larger average gene family size for the Calvin cycle relative to the photosystems.

The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

“…Indeed, parallel evidence from the study of patterns of gene retention following allo-polyploidization (Maere et al, 2005;Thomas et al, 2006;Coate et al, 2011) or from more manageable experimental systems like the X chromosome (Birchler, 2014) support the idea that dosage responses are selectively constrained by genetic pathways. This idea was formalized as the dosage balance hypothesis by Papp et al (2003), who argued that greater fitness loss would result from perturbing the relative abundance of components of a signaling cascade or of a multi-subunit protein complex than from absolute but concerted concentration changes that would maintain overall stoichiometry.…”

Comparative genomics and trait evolution in Cleomaceae, a model family for ancient polyploidy

“…Looking at several other species in which this is a confirmed and important phenomenon in gene family diversification Coate et al, 2011;Birchler and Veitia, 2014), we can assume that this effect has also played a role in the development of glucosinolate gene families in T. hassleriana.…”

“…An earlier study on the evolution of photosynthesis in soybean, showed that the Calvin-Benson-Bassham cycle (CBBC) and the light harvesting complex (LHC) gene families show a greater expansion from single gene duplications than both photosystem groups. This is explained by the increased dosage sensitivity of photosystem genes: if some subunits are expressed differently due to duplications while others are not, this is deleterious for the system as a whole (Coate et al, 2011). This acts as a conservation mechanism for gene copy number that does not affect the more loosely connected enzyme collection of the CBBC and LHC genes.…”

“…For a trait that is likely to be highly dosage sensitive (Coate et al, 2011), we expect that gene loss will be rare and that remnants from this old paleohexaploidy are still present. However, considering the time that has passed since the γ paleohexaploidy event and on the basis of absolute gene copy numbers some gene loss has taken place predating the transition from C3 to C4.…”

“…The contribution of WGD to photosynthesis-related genes has been studied in soybean, barrel-medic, Arabidopsis, and sorghum (Wang et al, 2009;Coate et al, 2011). The polyploid and non-polyploid duplicated gene retention in Glycine max, Medicago truncatula and Arabidopsis for four classes of photosynthesis-related genes was compared: the Calvin-Benson-Bassham-cycle (CBBC), the lightharvesting complex (LHC), photosystem I (PSI) and photosystem II (PSII).…”