Single‐parent expression drives dynamic gene expression complementation in maize hybrids

Li, Zhi; Zhou, Peng; Coletta, Rafael Della; Zhang, Tifu; Brohammer, Alex B.; O’Connor, Christine H.; Vaillancourt, Brieanne; Lipzen, Anna; Daum, Chris; Barry, Kerrie; León, Natalia de; Hirsch, Cory D.; Buell, C. Robin; Kaeppler, Shawn M.; Springer, Nathan M.

doi:10.1111/tpj.15042

Cited by 18 publications

(11 citation statements)

References 81 publications

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“…The dominance model, also known as the complementation model, describes the concept that deleterious alleles of different genes in both inbred lines are complemented in the F 1 -hybrid by beneficial alleles, which results in its superior phenotypic performance ( Jones, 1917 ). Recently, SPE complementation was demonstrated in genetically diverse maize genotypes along different stages of primary root development grown under controlled environmental conditions ( Baldauf et al, 2018 ) and in aboveground tissues ( Li et al, 2021 ). It was shown that non-syntenic genes were the driving force of gene expression complementation in hybrids ( Paschold et al, 2014 ; Marcon et al, 2017 ; Baldauf et al, 2018 ; Li et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

“…Recently, SPE complementation was demonstrated in genetically diverse maize genotypes along different stages of primary root development grown under controlled environmental conditions ( Baldauf et al, 2018 ) and in aboveground tissues ( Li et al, 2021 ). It was shown that non-syntenic genes were the driving force of gene expression complementation in hybrids ( Paschold et al, 2014 ; Marcon et al, 2017 ; Baldauf et al, 2018 ; Li et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

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Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids

et al. 2022

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The dominance model of heterosis explains the superior performance of F1 hybrids via the complementation of deleterious alleles by beneficial alleles in many genes. Genes active in one parent but inactive in the second lead to single-parent expression (SPE) complementation in maize (Zea mays L.) hybrids. In this study, SPE complementation resulted in ∼700 additionally active genes in different tissues of genetically diverse maize hybrids on average. We established that the number of SPE genes is significantly associated with mid-parent heterosis for all surveyed phenotypic traits. In addition, we highlighted that maternally (SPE_B) and paternally (SPE_X) active SPE genes enriched in gene co-expression modules are highly correlated within each SPE type but separated between these two SPE types. While SPE_B-enriched co-expression modules are positively correlated with phenotypic traits, SPE_X-enriched modules displayed a negative correlation. Gene Ontology (GO) term enrichment analyses indicated that SPE_B patterns are associated with growth and development, whereas SPE_X patterns are enriched in defense and stress response. In summary, these results link the degree of phenotypic mid-parent heterosis to the prevalence of gene expression complementation observed by SPE, supporting the notion that hybrids benefit from SPE complementation via its role in coordinating maize development in fluctuating environments.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids

et al. 2022

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“…For example, function complementation between dominant superior loci in hybrids has been reported to trigger heterosis in crops (5,6). In addition, single-parent expression has been found to be a general mechanism driving expression complementation in some hybrids (7)(8)(9). However, despite these findings, concurrent complementation of gene expression and biological function in a hybrid has rarely been reported, and it has remained a challenge to associate the genetic complementation in a hybrid with its heterotic phenotypes.…”

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confidence: 99%

Biological pathway expression complementation contributes to biomass heterosis in Arabidopsis

Liu

Deng

2021

Proc. Natl. Acad. Sci. U.S.A.

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The mechanisms underlying heterosis have long remained a matter of debate, despite its agricultural importance. How changes in transcriptional networks during plant development are relevant to the continuous manifestation of growth vigor in hybrids is intriguing and unexplored. Here, we present an integrated high-resolution analysis of the daily dynamic growth phenotypes and transcriptome atlases of young Arabidopsis seedlings (parental ecotypes [Col-0 and Per-1] and their F1 hybrid). Weighted gene coexpression network analysis uncovered divergent expression patterns between parents of the network hub genes, in which genes related to the cell cycle were more highly expressed in one parent (Col-0), whereas those involved in photosynthesis were more highly expressed in the other parent (Per-1). Notably, the hybrid exhibited spatiotemporal high-parent–dominant expression complementation of network hub genes in the two pathways during seedling growth. This suggests that the integrated capacities of cell division and photosynthesis contribute to hybrid growth vigor, which could be enhanced by temporal advances in the progression of leaf development in the hybrid relative to its parents. Altogether, this study provides evidence of expression complementation between fundamental biological pathways in hybrids and highlights the contribution of expression dominance in heterosis.

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“…Further, the genome assemblies of the six parents with annotation from a five-tissue transcriptome atlas (Li et al 2021; Bornowski et al 2021) are available for study, which increases the variety of opportunities for maize researchers. This population could be used to assay the effect of the alleles present within the population on combining ability, adaptation, genotype by environment interaction, stability, and provide a new paradigm for studying traditional and genomic selection.…”

Section: Discussionmentioning

confidence: 99%

Genetic mapping of flowering time and plant height in a maize Stiff Stalk MAGIC population

Michel

Lima

Hundley

et al. 2022

Preprint

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The Stiff Stalk heterotic pool is a foundation of US maize seed parent germplasm and has been heavily utilized by both public and private maize breeders since its inception in the 1930’s. Flowering time and plant height are critical characteristics for both inbred parents and their test crossed hybrid progeny. To study these traits, a six parent multiparent advanced generation intercross (MAGIC) population was developed including maize inbred lines B73, B84, PHB47 (B37 type), LH145 (B14 type), PHJ40 (novel early Stiff Stalk), and NKH8431 (B73/B14 type). A set of 779 doubled haploid lines were evaluated for flowering time and plant height in two field replicates in 2016 and 2017, and a subset of 689 and 561 doubled haploid lines were crossed to two testers, respectively, and evaluated as hybrids in two locations in 2018 and 2019 using an incomplete block design. Markers were derived from a Practical Haplotype Graph built from the founder whole genome assemblies and genotype-by-sequencing and exome capture-based sequencing of the population. Genetic mapping utilizing an update to R/qtl2 revealed differing profiles of significant loci for both traits between 636 of the DH lines and two sets of 571 and 472 derived hybrids. Genomic prediction was used to test the feasibility of predicting hybrid phenotypes based on the per se data. Predictive abilities were highest on direct models trained using the data they would predict (0.55 to 0.63), and indirect models trained using per se data to predict hybrid traits had slightly lower predictive abilities (0.49 to 0.55). Overall, this finding is consistent with the overlapping and non-overlapping significant QTL found within the per se and hybrid populations and suggests that selections for phenology traits can be made effectively on doubled haploid lines before hybrid data is available.Core IdeasA multi-parent advanced generation intercross (MAGIC) mapping population was developed from six founder Stiff Stalk maize inbreds with commercial relevance. Genetic mapping utilizing an update to R/qtl2 was demonstrated for flowering and plant height traits.Genetic mapping using maize inbred and hybrid information was compared and provided insight into trait expression in inbreds relative to heterotic testcross hybrids.

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Single‐parent expression drives dynamic gene expression complementation in maize hybrids

Cited by 18 publications

References 81 publications

Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids

Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids

Biological pathway expression complementation contributes to biomass heterosis in Arabidopsis

Genetic mapping of flowering time and plant height in a maize Stiff Stalk MAGIC population

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