Abstract
Main conclusion
Allele-specific expressed genes (ASEGs) are widespread in maize hybrid lines and play important roles of complementation of biological pathways in heterosis.
Abstract
Heterosis (hybrid vigor) is an important phenomenon with both theoretical and practical value. However, our understanding of the genetic and molecular mechanisms behind heterosis is still limited. Here, we analyzed a comprehensive dataset of maize (Zea mays L.), including RNA-seq data from three hybrid-parent triplets (HPTs) and acetylated protein data from one HPT. The gene expression patterns exhibited extensive variation between the hybrids and their parents, and a substantial number of allele-specific expressed genes (ASEGs) were identified in the hybrids. Notably, ASEGs from different HPTs were significantly enriched in various conserved pathways. The parental alleles of ASEGs with fewer deleterious single-nucleotide polymorphisms were more likely to be expressed in hybrid lines than other parental alleles. ASEGs were mainly enriched in the functional gene ontology terms protein biosynthesis, photosynthesis, and metabolism. In addition, the ASEGs across the three HPTs were involved in key photosynthetic pathways and might enhance the photosynthetic efficiency of the hybrids. These findings suggest that ASEGs involved in complementary biological pathways in maize hybrids contribute to heterosis, shedding new light on the molecular mechanism of heterosis.
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Data availability
Sequencing data have been deposited in the NCBI SRA database (accession number PRJNA861883).
Abbreviations
- ASEG:
-
Allele-specific expressed gene
- HPT:
-
Hybrid-parent triplet
- FDR:
-
False discovery rate
- SPE:
-
Single-parent expression
- IoU:
-
Intersection-over-Union
- SNP:
-
Single-nucleotide polymorphism
- MF:
-
Molecular function
- CC:
-
Cellular component
- BP:
-
Biological process
- GO:
-
Gene ontology
- KEGG:
-
Kyoto encyclopedia of genes and genomes
References
Baldauf JA, Liu M, Vedder L et al (2022) Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids. Plant Physiol 189:1625–1638. https://doi.org/10.1093/plphys/kiac180
Baldauf JA, Marcon C, Lithio A et al (2018) Single-parent expression is a general mechanism driving extensive complementation of non-syntenic genes in maize hybrids. Curr Biol 28:431-437.e4. https://doi.org/10.1016/j.cub.2017.12.027
Belting H-G, Shashikant CS, Ruddle FH (1998) Modification of expression and cis-regulation of Hoxc8 in the evolution of diverged axial morphology. Proc Natl Acad Sci USA 95:2355–2360. https://doi.org/10.1073/pnas.95.5.2355
Birchler JA, Yao H, Chudalayandi S et al (2010) Heterosis. Plant Cell 22:2105–2112. https://doi.org/10.1105/tpc.110.076133
Birdseye D, de Boer LA, Bai H et al (2021) Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins. Proc Natl Acad Sci USA 118:e2109332118. https://doi.org/10.1073/pnas.2109332118
Botet R, Keurentjes JJB (2020) The role of transcriptional regulation in hybrid vigor. Front Plant Sci 11:410. https://doi.org/10.3389/fpls.2020.00410
Bruce AB (1910) The mendelian theory of heredity and the augmentation of vigor. Science 32:627–628. https://doi.org/10.1126/science.32.827.627-a
Chen L, Bian J, Shi S et al (2018a) Genetic analysis for the grain number heterosis of a super-hybrid rice WFYT025 combination using RNA-seq. Rice 11:37. https://doi.org/10.1186/s12284-018-0229-y
Chen Y, Zhou Q, Tian R et al (2018b) Proteomic analysis reveals that auxin homeostasis influences the eighth internode length heterosis in maize (Zea mays). Sci Rep 8:7159. https://doi.org/10.1038/s41598-018-23874-6
Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15:57. https://doi.org/10.1016/j.tplants.2009.12.003
Cingolani P, Platts A, Wang LL et al (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly (austin) 6:80–92. https://doi.org/10.4161/fly.19695
Cookson W, Liang L, Abecasis G et al (2009) Map** complex disease traits with global gene expression. Nat Rev Genet 10:184–194. https://doi.org/10.1038/nrg2537
Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26:1367–1372. https://doi.org/10.1038/nbt.1511
Darwin C (1876) The effects of cross and self-fertilization in the vegetable kingdom. John Murray, London
Doust AN, Lukens L, Olsen KM et al (2014) Beyond the single gene: How epistasis and gene-by-environment effects influence crop domestication. Proc Natl Acad Sci USA 111:6178–6183. https://doi.org/10.1073/pnas.1308940110
Fan J, Hu J, Xue C et al (2020) ASEP: Gene-based detection of allele-specific expression across individuals in a population by RNA sequencing. PLoS Genet 16(5):e1008786. https://doi.org/10.1371/journal.pgen.1008786
Freed D, Aldana R, Weber JA, Edwards JS (2017) The sentieon genomics tools - a fast and accurate solution to variant calling from next-generation sequence data. BioRxiv. https://doi.org/10.1101/115717
Guo X, Guo Y, Ma J et al (2013) Map** heterotic loci for yield and agronomic traits using chromosome segment introgression lines in cotton. J Integr Plant Biol 55:759–774. https://doi.org/10.1111/jipb.12054
Hochholdinger F, Baldauf JA (2018) Heterosis in plants. Curr Biol 28:1089–1092. https://doi.org/10.1016/j.cub.2018.06.041
Hua J, **ng Y, Wu W et al (2003) Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 100:2574–2579. https://doi.org/10.1073/pnas.0437907100
Huang X, Yang S, Gong J et al (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537:629–633. https://doi.org/10.1038/nature19760
Jones DF (1917) Dominance of linked factors as a means of accounting for heterosis. Proc Natl Acad Sci USA 3:310–312. https://doi.org/10.1073/pnas.3.4.310
Kaeppler S (2012) Heterosis: many genes, many mechanisms—end the search for an undiscovered unifying theory. ISRN Bot 2012:e682824. https://doi.org/10.5402/2012/682824
Karasov TL, Chae E, Herman JJ, Bergelson J (2017) Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29:666–680. https://doi.org/10.1105/tpc.16.00931
Li H, Yang Q, Gao L et al (2017) Identification of heterosis-associated stable QTLs for ear-weight-related traits in an elite maize hybrid Zhengdan 958 by Design III. Front Plant Sci 8:1367–1372. https://doi.org/10.3389/fpls.2017.00561
Li X, Li X, Fridman E et al (2015) Dissecting repulsion linkage in the dwarfing gene Dw3 region for sorghum plant height provides insights into heterosis. Proc Natl Acad Sci USA 112:11823–11828. https://doi.org/10.1073/pnas.1509229112
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930. https://doi.org/10.1093/bioinformatics/btt656
Lim K-S, Chang S-S, Choi B-H et al (2019) Genome-wide analysis of allele-specific expression patterns in seventeen tissues of korean cattle (Hanwoo). Animals 9:727. https://doi.org/10.3390/ani9100727
Lin Z, Qin P, Zhang X et al (2020) Divergent selection and genetic introgression shape the genome landscape of heterosis in hybrid rice. Proc Natl Acad Sci USA 117:4623–4631. https://doi.org/10.1073/pnas.1919086117
Liu H, Wang Q, Chen M et al (2020) Genome-wide identification and analysis of heterotic loci in three maize hybrids. Plant Biotechnol J 18:185–194. https://doi.org/10.1111/pbi.13186
Liu W, He G, Deng XW (2021) Biological pathway expression complementation contributes to biomass heterosis in Arabidopsis. Proc Natl Acad Sci USA 118:e2023278118. https://doi.org/10.1073/pnas.2023278118
Liu Z, Dong X, Li Y (2018) A Genome-wide study of allele-specific expression in colorectal cancer. Front Genet 9:570. https://doi.org/10.3389/fgene.2018.00570
Liu Q, Zhou Y, Morrell PL, Gaut BS (2017) Deleterious variants in asian rice and the potential cost of domestication. Mol Biol Evol 34:908–924. https://doi.org/10.1093/molbev/msw296
Miller M, Song Q, Shi X et al (2015) Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis. Nat Commun 6:7453. https://doi.org/10.1038/ncomms8453
Morgan M, Shepherd L (2022) AnnotationHub: Client to access AnnotationHub resources. R Package version 3.4.0., Bioconductor
Narita T, Weinert BT, Choudhary C (2019) Functions and mechanisms of non-histone protein acetylation. Nat Rev Mol Cell Biol 20:156–174. https://doi.org/10.1038/s41580-018-0081-3
Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11:R25. https://doi.org/10.1186/gb-2010-11-3-r25
Rockenbach MF, Corrêa CCG, Heringer AS et al (2018) Differentially abundant proteins associated with heterosis in the primary roots of popcorn. PLoS ONE 13:e0197114. https://doi.org/10.1371/journal.pone.0197114
Shao L, **ng F, Xu C et al (2019) Patterns of genome-wide allele-specific expression in hybrid rice and the implications on the genetic basis of heterosis. Proc Natl Acad Sci USA 116:5653–5658. https://doi.org/10.1073/pnas.1820513116
Shen W, Le S, Li Y, Hu F (2016) SeqKit: A cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE 11:e0163962. https://doi.org/10.1371/journal.pone.0163962
Shen Y, Sun S, Hua S et al (2017) Analysis of transcriptional and epigenetic changes in hybrid vigor of allopolyploid Brassica napus uncovers key roles for small RNAs. Plant J 91:874–893. https://doi.org/10.1111/tpj.13605
Shull GH (1908) The composition of a field of maize. J Heredity 4:296–301. https://doi.org/10.1093/jhered/os-4.1.296
Shvedunova M, Akhtar A (2022) Modulation of cellular processes by histone and non-histone protein acetylation. Nat Rev Mol Cell Biol 23:329–349. https://doi.org/10.1038/s41580-021-00441-y
Song Q, Ando A, Xu D et al (2018) Diurnal down-regulation of ethylene biosynthesis mediates biomass heterosis. Proc Natl Acad Sci USA 115:5606–5611. https://doi.org/10.1073/pnas.1722068115
Song X, Ni Z, Yao Y et al (2009) Identification of differentially expressed proteins between hybrid and parents in wheat (Triticum aestivum L.) seedling leaves. Theor Appl Genet 118:213–225. https://doi.org/10.1007/s00122-008-0890-4
Thimm O, Bläsing O, Gibon Y et al (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939. https://doi.org/10.1111/j.1365-313X.2004.02016.x
Wang R-L, Stec A, Hey J et al (1999) The limits of selection during maize domestication. Nature 398:236–239. https://doi.org/10.1038/18435
Wu T, Hu E, Xu S et al (2021) clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. The Innovation. https://doi.org/10.1016/j.xinn.2021.100141
**ao J, Li J, Yuan L, Tanksley SD (1995) Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. Genetics 140:745–754. https://doi.org/10.1093/genetics/140.2.745
**ao Y, Jiang S, Cheng Q, Wang X (2021) The genetic mechanism of heterosis utilization in maize improvement. Genome Biol 22:148. https://doi.org/10.1186/s13059-021-02370-7
Yang J, Mezmouk S, Baumgarten A et al (2017) Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize. PLoS Genet 13:e1007019. https://doi.org/10.1371/journal.pgen.1007019
Yang L, Liu P, Wang X et al (2021) A central circadian oscillator confers defense heterosis in hybrids without growth vigor costs. Nat Commun 12:2317. https://doi.org/10.1038/s41467-021-22268-z
Yi G, Shin H, Park HR et al (2020) Revealing biomass heterosis in the allodiploid xBrassicoraphanus, a hybrid between Brassica rapa and Raphanus sativus, through integrated transcriptome and metabolites analysis. BMC Plant Biol 20:252. https://doi.org/10.1186/s12870-020-02470-9
Zhou P, Hirsch CN, Briggs SP, Springer NM (2019) Dynamic patterns of gene expression additivity and regulatory variation throughout maize development. Mol Plant 12:410–425. https://doi.org/10.1016/j.molp.2018.12.015
Acknowledgements
This research was supported by Hainan Yazhou Bay Seed Lab (B21HJ8102), the Major Program of Hubei Hongshan Laboratory (2021hszd008), the Huazhong Agricultural University Scientific & Technological Self-innovation Foundation (2021ZKPY001), and the Agricultural Science and Technology Innovation Program of CAAS.
Funding
This research was supported by Hainan Yazhou Bay Seed Lab (B21HJ8102), the Major Program of Hubei Hongshan Laboratory (2021hszd008), Huazhong Agricultural University Scientific & Technological Self-innovation Foundation (2021ZKPY001), and the Agricultural Science and Technology Innovation Program of CAAS.
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Zhou, T., Afzal, R., Haroon, M. et al. Dominant complementation of biological pathways in maize hybrid lines is associated with heterosis. Planta 256, 111 (2022). https://doi.org/10.1007/s00425-022-04028-5
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DOI: https://doi.org/10.1007/s00425-022-04028-5