Transcriptomic plasticity of maize hybrids and their parental inbred lines at the interface of genotype and development
Final Report Abstract
F1-hybrids are more vigorous than their homozygous, genetically distinct parents, a phenomenon known as heterosis. In the present DFG project, we discovered that an extreme instance of gene expression complementation is widespread in maize. We designated the observation that hundreds of maize genes are active in only one of the two parental inbred lines as single parent expression (SPE) and demonstrated that these genes are almost always active in the corresponding F1-hybrids. This type of gene expression complementation is consistent with the dominance model for heterosis. Only a small fraction of SPE patterns are due to genomic presence absence variations i.e. that lack of these genes in one genotype. In most instances, only the allele active in one inbred line was active in the hybrid. Our initial study was executed in whole seedling roots of the genotypes B73 and Mo17 and their reciprocal hybrids. In follow up experiments, we surveyed how the genetic divergence of these two maize inbred lines affects the transcriptomic landscape in four different primary root tissues of its F1-hybrid progeny. We observed in all tissues hundreds of SPE patterns. As a consequence, the number of active genes in hybrids exceeded that of their parents in each tissue by >400. SPE patterns are highly dynamic as illustrated by their excessive degree of tissue-specificity (80%). The biological significance of this type of complementation is underpinned by the observation that a disproportionally high number of SPE genes is nonsyntenic – as opposed to all expressed genes. Non-syntenic genes likely evolved after the last whole genome duplication and are therefore younger than the syntenic genes. Moreover, we demonstrated that SPE patterns are substantially more stable to expression changes by water deficit treatment than other genotype-specific expression profiles. Subsequently, we extended our analysis to a distantly related panel of homozygous maize inbred lines and to three different stages of root development. We observed on average ~1,000 SPE patterns for all inbred line combinations during primary root development. By this analysis, we demonstrated that extreme expression complementation is a general mechanism that results in hundreds of additionally active genes and their encoded biological functions in hybrids. We also demonstrated that non-syntenic genes are the driving force of gene expression complementation in hybrids in all surveyed instances. Among those, the highly diversified families of bZIP and bHLH transcription factors were systematically overrepresented. In summary, we demonstrated that extreme gene expression complementation extensively shapes the transcriptomic plasticity of maize hybrids and might therefore be one factor controlling the developmental plasticity of hybrids.
Publications
- (2012) Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents. Genome Res 22: 2445-2454
Paschold A, Jia Y, Marcon C, Lund S, Larson NB, Yeh CT, Ossowski S, Lanz C, Nettleton D, Schnable PS, Hochholdinger F
(See online at https://doi.org/10.1101/gr.138461.112) - (2013) Heterosis-associated proteome analyses of maize (Zea mays L.) seminal roots by quantitative label-free LC-MS. J. Proteomics 93: 295-302
Marcon C, Lamkemeyer T, Malik WA, Ungrue D, Piepho H-P, Hochholdinger F
(See online at https://doi.org/10.1016/j.jprot.2013.04.015) - (2014) Non-syntenic genes drive highly dynamic complementation of gene expression in maize hybrids. Plant Cell 26: 3939-3948
Paschold A, Larson NB, Marcon C, Schnable JC, Yeh CT, Lanz C, Nettleton D, Piepho HP, Schnable PS, Hochholdinger F
(See online at https://doi.org/10.1105/tpc.114.130948) - (2016) Nonsyntenic genes drive tissuespecific dynamics of differential, nonadditive and allelic expression patterns in maize hybrids. Plant Physiol 171: 1144-1155
Baldauf JA, Marcon C, Paschold A, Hochholdinger F
(See online at https://doi.org/10.1104/pp.16.00262) - (2017) Stability of single parent gene expression complementation in maize hybrids upon water deficit stress. Plant Physiol 173: 1247-1257
Marcon C, Paschold A, Malik WA, Lithio A, Baldauf JA, Altrogge L, Opitz N, Lanz C, Schoof H, Nettleton D, Piepho H-P, Hochholdinger F
(See online at https://doi.org/10.1104/pp.16.01045) - (2018) Heterosis in Crop Plants. Cur Biol 28: R1089-R1092
Hochholdinger F, Baldauf JA
(See online at https://doi.org/10.1016/j.cub.2018.06.041) - (2018) Proteomics of Maize Root Development. Front Plant Sci 9: 143
Hochholdinger F, Marcon C, Baldauf JA, Frey F, Yu P
(See online at https://doi.org/10.3389/fpls.2018.00143) - (2018) Single parent expression is a general mechanism that drives extensive complementation of non-syntenic genes in maize (Zea mays L.) hybrids. Curr Biol 28: 431-437
Baldauf JA, Marcon C, Lithio A, Vedder L, Altrogge L, Piepho H-P, Schoof H, Nettleton D, Hochholdinger F
(See online at https://doi.org/10.1016/j.cub.2017.12.027) - (2018) Transcriptomic dissection of maize root system development. Compendium of plant genomes: The Zea mays Genome. 1st ed. (eds. J. Bennetzen, S. Flint-Garcia, C. Hirsch and R. Tuberosa) pp. 247-257. Springer Nature
Yu P, Marcon C, Baldauf JA, Frey F, Baer M, Hochholdinger F
(See online at https://doi.org/10.1007/978-3-319-97427-9_15)
