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1. Absence of heterosis for hypoxia tolerance in F1 hybrids of Tigriopus californicus

   https://doi.org/10.1093/jhered/esae061  

   Deconinck, Aimee; Madalone, Olivia F; Willett, Christopher S (October 2024, Journal of Heredity)

   Delmore, Kira (Ed.)

   Abstract Hybridization produces a range of outcomes from advantageous to disadvantageous, and a goal of genetic research is to understand the gene interactions that generate these outcomes. Interactions between cytoplasmic elements, such as mitochondria, and the nucleus may be particularly vulnerable to accruing disadvantageous combinations as a result of their different rates of evolution. Consequently, mitonuclear incompatibilities may play an important role in hybrid outcomes even if their negative impacts could be masked for some fitness measures by heterosis in first-generation (F1) hybrids. We used Tigriopus californicus, a model system for mitonuclear incompatibilities that is also known for exhibiting heterosis in the F1 generation and outbreeding depression in later generations, to test whether heterosis or outbreeding depression would occur when mitonuclear mismatch was paired with a stress that heavily impacts mitochondrial processes—specifically, hypoxia. We generated 284 parental and 436 F1 hybrids from four population crosses (720 total) and compared parental and F1 populations for hypoxia tolerance. We observed that, on average, F1 hybrids were less likely to survive a hypoxia stress test than parental populations, although we did not detect a statistically significant trend (P = 0.246 to 0.614). This suggests that hypoxia may be a particularly intense stressor for mitonuclear coordination and hybridization outcomes vary by trait. 

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2. Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

   https://doi.org/10.1093/genetics/iyad114  

   Bird, Kevin A; Pires, J Chris; VanBuren, Robert; Xiong, Zhiyong; Edger, Patrick P (June 2023, GENETICS)

   Bomblies, K (Ed.)

   The gene balance hypothesis proposes that selection acts on the dosage (i.e. copy number) of genes within dosage-sensitive portions of networks, pathways, and protein complexes to maintain balanced stoichiometry of interacting proteins, because perturbations to stoichiometric balance can result in reduced fitness. This selection has been called dosage balance selection. Dosage balance selection is also hypothesized to constrain expression responses to dosage changes, making dosage-sensitive genes (those encoding members of interacting proteins) experience more similar expression changes. In allopolyploids, where whole-genome duplication involves hybridization of diverged lineages, organisms often experience homoeologous exchanges that recombine, duplicate, and delete homoeologous regions of the genome and alter the expression of homoeologous gene pairs. Although the gene balance hypothesis makes predictions about the expression response to homoeologous exchanges, they have not been empirically tested. We used genomic and transcriptomic data from 6 resynthesized, isogenic Brassica napus lines over 10 generations to identify homoeologous exchanges, analyzed expression responses, and tested for patterns of genomic imbalance. Groups of dosage-sensitive genes had less variable expression responses to homoeologous exchanges than dosage-insensitive genes, a sign that their relative dosage is constrained. This difference was absent for homoeologous pairs whose expression was biased toward the B. napus A subgenome. Finally, the expression response to homoeologous exchanges was more variable than the response to whole-genome duplication, suggesting homoeologous exchanges create genomic imbalance. These findings expand our knowledge of the impact of dosage balance selection on genome evolution and potentially connect patterns in polyploid genomes over time, from homoeolog expression bias to duplicate gene retention. 

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3. Microbe-dependent heterosis in maize

   https://doi.org/10.1073/pnas.2021965118  

   Wagner, Maggie R.; Tang, Clara; Salvato, Fernanda; Clouse, Kayla M.; Bartlett, Alexandria; Vintila, Simina; Phillips, Laura; Sermons, Shannon; Hoffmann, Mark; Balint-Kurti, Peter J.; et al (July 2021, Proceedings of the National Academy of Sciences)

   Hybrids account for nearly all commercially planted varieties of maize and many other crop plants because crosses between inbred lines of these species produce first-generation [F₁] offspring that greatly outperform their parents. The mechanisms underlying this phenomenon, called heterosis or hybrid vigor, are not well understood despite over a century of intensive research. The leading hypotheses—which focus on quantitative genetic mechanisms (dominance, overdominance, and epistasis) and molecular mechanisms (gene dosage and transcriptional regulation)—have been able to explain some but not all of the observed patterns of heterosis. Abiotic stressors are known to impact the expression of heterosis; however, the potential role of microbes in heterosis has largely been ignored. Here, we show that heterosis of root biomass and other traits in maize is strongly dependent on the belowground microbial environment. We found that, in some cases, inbred lines perform as well by these criteria as their F₁offspring under sterile conditions but that heterosis can be restored by inoculation with a simple community of seven bacterial strains. We observed the same pattern for seedlings inoculated with autoclaved versus live soil slurries in a growth chamber and for plants grown in steamed or fumigated versus untreated soil in the field. In a different field site, however, soil steaming increased rather than decreased heterosis, indicating that the direction of the effect depends on community composition, environment, or both. Together, our results demonstrate an ecological phenomenon whereby soil microbes differentially impact the early growth of inbred and hybrid maize. 

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4. Diverse modes of gene action contribute to heterosis for quantitative disease resistance in maize

   https://doi.org/10.1093/genetics/iyaf049  

   Hudson, Asher I; Wagner, Maggie R; Sermons, Shannon; Balint-Kurti, Peter J (March 2025, GENETICS)

   Yuan, Y (Ed.)

   Abstract Disease resistance in plants can be conferred by single genes of large effect or by multiple genes each conferring incomplete resistance. The latter case, termed quantitative resistance, may be difficult for pathogens to overcome through evolution due to the low selection pressures exerted by the actions of any single gene and, for some diseases, is the only identified source of genetic resistance. We evaluated quantitative resistance to 2 diseases of maize in a biparental mapping population as well as backcrosses to both parents. Quantitative trait locus analysis shows that the genetic architecture of resistance to these diseases is characterized by several modes of gene action including additivity as well as dominance, overdominance, and epistasis. Heterosis or hybrid vigor, the improved performance of a hybrid compared with its parents, can be caused by nonadditive gene action and is fundamental to the breeding of several crops including maize. In the backcross populations and a diverse set of maize hybrids, we find heterosis for resistance in many cases and that the degree of heterosis appears to be dependent on both hybrid genotype and disease. 

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5. The conservation value of small population remnants: Variability in inbreeding depression and heterosis of a perennial herb, the narrow-leaved purple coneflower (Echinacea angustifolia)

   https://doi.org/10.1093/jhered/esae055  

   Thoen, Riley D; Southgate, Andrea; Kiefer, Gretel; Shaw, Ruth G; Wagenius, Stuart (October 2024, Journal of Heredity)

   Anthropogenically fragmented populations may have reduced fitness due to loss of genetic diversity and inbreeding. The extent of such fitness losses due to fragmentation and potential gains from conservation actions are infrequently assessed together empirically. Controlled crosses within and among populations can identify whether populations are at risk of inbreeding depression and whether inter-population crossing alleviates fitness loss. Because fitness depends on the environment and life stage, studies quantifying cumulative fitness over a large portion of the lifecycle in conditions that mimic natural environments are most informative. To assess the fitness consequences of habitat fragmentation, we leveraged controlled within-family, within-population, and between-population crosses to quantify inbreeding depression and heterosis in seven populations of Echinacea angustifolia within a 6,400-ha area. We then assessed cumulative offspring fitness after 14 yr of growth in a natural experimental plot (N = 1,136). The mean fitness of progeny from within-population crosses varied considerably, indicating genetic differentiation among source populations, even though these sites are all less than 9 km apart. The fitness consequences of within-family and between-population crosses varied in magnitude and direction. Only one of the seven populations showed inbreeding depression of high effect, while four populations showed substantial heterosis. Outbreeding depression was rare and slight. Our findings indicate that local crossings between isolated populations yield unpredictable fitness consequences ranging from slight decreases to substantial increases. Interestingly, inbreeding depression and heterosis did not relate closely to population size, suggesting that all fragmented populations could contribute to conservation goals as either pollen recipients or donors. 

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