Improved redox homeostasis owing to the up-regulation of one-carbon metabolism and related pathways is crucial for yeast heterosis at high temperature

Abstract

Heterosis or hybrid vigor is a common phenomenon in plants and animals; however, the molecular mechanisms underlying heterosis remain elusive, despite extensive studies on the phenomenon for more than a century. Here we constructed a large collection of F1 hybrids of Saccharomyces cerevisiae by spore-to-spore mating between homozygous wild strains of the species with different genetic distances and compared growth performance of the F1 hybrids with their parents. We found that heterosis was prevalent in the F1 hybrids at 40°C. A hump-shaped relationship between heterosis and parental genetic distance was observed. We then analyzed transcriptomes of selected heterotic and depressed F1 hybrids and their parents growing at 40°C and found that genes associated with one-carbon metabolism and related pathways were generally up-regulated in the heterotic F1 hybrids, leading to improved cellular redox homeostasis at high temperature. Consistently, genes related with DNA repair, stress responses, and ion homeostasis were generally down-regulated in the heterotic F1 hybrids. Furthermore, genes associated with protein quality control systems were also generally down-regulated in the heterotic F1 hybrids, suggesting a lower level of protein turnover and thus higher energy use efficiency in these strains. In contrast, the depressed F1 hybrids, which were limited in number and mostly shared a common aneuploid parental strain, showed a largely opposite gene expression pattern to the heterotic F1 hybrids. We provide new insights into molecular mechanisms underlying heterosis and thermotolerance of yeast and new clues for a better understanding of the molecular basis of heterosis in plants and animals.

Highly diverged lineages of Saccharomyces paradoxus in temperate to subtropical climate zones in China

“…However, in our opinion, this phenomenon needs to be confirmed. In contrast to our recent study (Song et al, 2021), Bernardes et al (2017) did not observe significant heterosis in intraspecific hybrids of S. cerevisiae either.…”

Evidence of myomiR regulation of the pentose phosphate pathway during mechanical load‐induced hypertrophy

“…Furthermore, oxidative modifications can occur on ribosomal proteins and ribosome modifying enzymes which may interfere with translation (Shcherbik & Pestov, 2019 ). NADPH production could also attenuate errors in protein synthesis by reducing the abundance of free radicals that would otherwise cause expression of genes associated with DNA damage, oxidized mRNA, and proteolysis (Song et al, 2021 ). Altogether, increasing NADPH to reduce oxidative stress could allow for the high rate of protein synthesis that occurs during MOV and suggests that modulating NADPH could lead to improvements in protein synthesis.…”

The Ecology and Evolution of the Baker’s Yeast Saccharomyces cerevisiae

“…Heterozygous yeast cells are usually more vigorous than homozygous cells in growth and stress tolerance because of heterosis, or hybrid vigor [ 41 , 93 , 94 , 95 , 96 , 97 ]. Recently, Song et al [ 98 ] showed that thermotolerant heterosis is prevalent in the F1 hybrids formed by spore-to-spore mating of different wild S. cerevisiae strains. The hybrids can usually cope with oxidative stress more effectively by up-regulation of their one-carbon metabolism and related pathways, leading to reduced DNA and protein damage and higher energy use efficiency.…”

“…Tolerance to high osmolarity, temperature, ethanol concentration, and ROS level is required for domesticated strains [ 92 ]. A recent study showed that heterosis contributes to high-temperature tolerance of domesticated S. cerevisiae [ 98 ], while another study showed that artificial hybrids of S. paradoxus did not show heterosis [ 129 ], implying heterozygosity may not contribute to the fitness of this species. Indeed, heterozygous strains of S. paradoxus and other non- cerevisiae Saccharomyces species have rarely been found in nature or man-made environments, though inter-species hybrids of Saccharomyces species are not uncommon in industrial yeast strains [ 101 , 128 , 130 ].…”