Sporophyte Stage Genes Exhibit Stronger Selection Than Gametophyte Stage Genes in Haplodiplontic Giant Kelp

Gary Molano,Jose Diesel,Filipe Alberto,Sergey V. Nuzhdin,Gabriel J. Montecinos

doi:10.3389/fmars.2021.774076

Abstract

Macrocystis pyrifera (giant kelp), a haplodiplontic brown macroalga that alternates between a macroscopic diploid (sporophyte) and a microscopic haploid (gametophyte) phase, provides an ideal system to investigate how ploidy background affects the evolutionary history of a gene. In M. pyrifera, the same genome is subjected to different selective pressures and environments as it alternates between haploid and diploid life stages. We assembled M. pyrifera gene models using available expression data and validated 8,292 genes models using the model alga Ectocarpus siliculosus. Differential expression analysis identified gene models expressed in either or both the haploid and diploid life stages while functional annotation identified processes enriched in each stage. Genes expressed preferentially or exclusively in the gametophyte stage were found to have higher nucleotide diversity (π = 2.3 × 10–3 and 2.8 × 10–3, respectively) than those for sporophytes (π = 1.1 × 10–3 and 1 × 10–3, respectively). While gametophyte-biased genes show faster sequence evolution, the sequence evolution exhibits less signatures of adaptations when compared to sporophyte-biased genes. Our findings contrast the standing masking hypothesis, which predicts higher standing genetic variation at the sporophyte stage, and support the strength of expression theory, which posits that genes expressed more strongly are expected to evolve slower. We argue that the sporophyte stage undergoes more stringent selection compared with the gametophyte stage, which carries a heavy genetic load associated with broadcast spawning. Furthermore, using whole-genome sequencing, we confirm the strong population structure in wild M. pyrifera populations previously established using microsatellite markers, and estimate population genetic parameters, such as pairwise genetic diversity and Tajima’s D, important for conservation and domestication of M. pyrifera.

Highlights

The early evolutionary theory of “masking” posits that ploidy will affect the rates of selection on genes (Crow and Kimura, 1965)
Our findings suggest that gene strength of expression in M. pyrifera was a major factor for sequence evolution, as genes expressed in the sporophyte stage had higher levels of average expression and showed more adaptive evolution than genes expressed ubiquitously or in the gametophyte stage
This study has set the stage for future work with giant kelp that will greatly benefit both conservation and domestication efforts by establishing important population genetic parameters such pairwise genetic diversity, Tajima’s D, and dN/dS using gene models

Summary

Introduction

The early evolutionary theory of “masking” posits that ploidy will affect the rates of selection on genes (Crow and Kimura, 1965). Masking increases the genetic diversity of the diploid species, as deleterious alleles persist far longer than in haploid species and carry the potential to be beneficial in varying environmental conditions (Raper and Flexer, 1970). Haploids are unmasked in comparison to diploids: with only a single copy of each allele, haploids are more exposed to selection, meaning that beneficial mutations reach fixation and deleterious alleles are purged faster (Kondrashov and Crow, 1991; Otto and Gerstein, 2008). Masking theory predicts that diploid-specific genes should contain more genetic variation than haploid genes, as diploid-specific genes are not exposed to selection pressure in the haploid stage and will accumulate mutations, while recessive mutations will be quickly purged from haploid-specific genes (Szövényi et al, 2013)

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