An Epigenetic Basis of Inbreeding Depression in Maize

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2021 Aug 28

PMID 34452913

Citations 14

Authors

Tongwen Han

Fang Wang

Qingxin Song

Wenxue Ye

Tieshan Liu

Liming Wang

Z Jeffrey Chen

Affiliations

Soon will be listed here.

Abstract

Inbreeding depression is widespread across plant and animal kingdoms and may arise from the exposure of deleterious alleles and/or loss of overdominant alleles resulting from increased homozygosity, but these genetic models cannot fully explain the phenomenon. Here, we report epigenetic links to inbreeding depression in maize. Teosinte branched1/cycloidea/proliferating cell factor (TCP) transcription factors control plant development. During successive inbreeding among inbred lines, thousands of genomic regions across TCP-binding sites (TBS) are hypermethylated through the H3K9me2-mediated pathway. These hypermethylated regions are accompanied by decreased chromatin accessibility, increased levels of the repressive histone marks H3K27me2 and H3K27me3, and reduced binding affinity of maize TCP-proteins to TBS. Consequently, hundreds of TCP-target genes involved in mitochondrion, chloroplast, and ribosome functions are down-regulated, leading to reduced growth vigor. Conversely, random mating can reverse corresponding hypermethylation sites and TCP-target gene expression, restoring growth vigor. These results support a unique role of reversible epigenetic modifications in inbreeding depression.

Citing Articles

Transcriptional regulatory network reveals key transcription factors for regulating agronomic traits in soybean.

Jiao W, Wang M, Guan Y, Guo W, Zhang C, Wei Y Genome Biol. 2024; 25(1):313.

PMID: 39695844 PMC: 11656900. DOI: 10.1186/s13059-024-03454-w.

Genome-Wide Diversity in Lowland and Highland Maize Landraces From Southern South America: Population Genetics Insights to Assist Conservation.

Dominguez P, Gutierrez A, Fass M, Filippi C, Vera P, Puebla A Evol Appl. 2024; 17(12):e70047.

PMID: 39628628 PMC: 11609054. DOI: 10.1111/eva.70047.

The evolutionary ecology of inbreeding depression in wild plant populations and its impact on plant mating systems.

Cheptou P Front Plant Sci. 2024; 15:1359037.

PMID: 39315378 PMC: 11416937. DOI: 10.3389/fpls.2024.1359037.

Promises and challenges of crop translational genomics.

Mascher M, Jayakodi M, Shim H, Stein N Nature. 2024; 636(8043):585-593.

PMID: 39313530 PMC: 7616746. DOI: 10.1038/s41586-024-07713-5.

Functional Characterization of Accessible Chromatin in Common Wheat.

Zheng D, Lin K, Yang X, Zhang W, Cheng X Int J Mol Sci. 2024; 25(17).

PMID: 39273331 PMC: 11395023. DOI: 10.3390/ijms25179384.

References

Song Q, Huang T, Yu H, Ando A, Mas P, Ha M . Diurnal regulation of SDG2 and JMJ14 by circadian clock oscillators orchestrates histone modification rhythms in Arabidopsis. Genome Biol. 2019; 20(1):170. PMC: 6892391. DOI: 10.1186/s13059-019-1777-1. View

Hollister J, Gaut B . Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 2009; 19(8):1419-28. PMC: 2720190. DOI: 10.1101/gr.091678.109. View

Lu X, Hu X, Zhao Y, Song W, Zhang M, Chen Z . Map-based cloning of zb7 encoding an IPP and DMAPP synthase in the MEP pathway of maize. Mol Plant. 2012; 5(5):1100-12. DOI: 10.1093/mp/sss038. View

Zhang C, Wang P, Tang D, Yang Z, Lu F, Qi J . The genetic basis of inbreeding depression in potato. Nat Genet. 2019; 51(3):374-378. DOI: 10.1038/s41588-018-0319-1. View

Venney C, Johansson M, Heath D . Inbreeding effects on gene-specific DNA methylation among tissues of Chinook salmon. Mol Ecol. 2016; 25(18):4521-33. DOI: 10.1111/mec.13777. View

Saze H, Shiraishi A, Miura A, Kakutani T . Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science. 2008; 319(5862):462-5. DOI: 10.1126/science.1150987. View

JONES D . Continued Inbreeding in Maize. Genetics. 1939; 24(4):462-73. PMC: 1209049. DOI: 10.1093/genetics/24.4.462. View

Clark R, Wagler T, Quijada P, Doebley J . A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet. 2006; 38(5):594-7. DOI: 10.1038/ng1784. View

Yao H, Srivastava S, Swyers N, Han F, Doerge R, Birchler J . Inbreeding Depression in Genotypically Matched Diploid and Tetraploid Maize. Front Genet. 2020; 11:564928. PMC: 7734256. DOI: 10.3389/fgene.2020.564928. View

10.

Fu F, Dawe R, Gent J . Loss of RNA-Directed DNA Methylation in Maize Chromomethylase and DDM1-Type Nucleosome Remodeler Mutants. Plant Cell. 2018; 30(7):1617-1627. PMC: 6096594. DOI: 10.1105/tpc.18.00053. View

11.

Bailey T, Boden M, Buske F, Frith M, Grant C, Clementi L . MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009; 37(Web Server issue):W202-8. PMC: 2703892. DOI: 10.1093/nar/gkp335. View

12.

Ng D, Miller M, Yu H, Huang T, Kim E, Lu J . A Role for CHH Methylation in the Parent-of-Origin Effect on Altered Circadian Rhythms and Biomass Heterosis in Arabidopsis Intraspecific Hybrids. Plant Cell. 2014; 26(6):2430-2440. PMC: 4114943. DOI: 10.1105/tpc.113.115980. View

13.

Rodgers-Melnick E, Vera D, Bass H, Buckler E . Open chromatin reveals the functional maize genome. Proc Natl Acad Sci U S A. 2016; 113(22):E3177-84. PMC: 4896728. DOI: 10.1073/pnas.1525244113. View

14.

Bass J, Takahashi J . Circadian integration of metabolism and energetics. Science. 2010; 330(6009):1349-54. PMC: 3756146. DOI: 10.1126/science.1195027. View

15.

Rigal M, Becker C, Pelissier T, Pogorelcnik R, Devos J, Ikeda Y . Epigenome confrontation triggers immediate reprogramming of DNA methylation and transposon silencing in Arabidopsis thaliana F1 epihybrids. Proc Natl Acad Sci U S A. 2016; 113(14):E2083-92. PMC: 4833259. DOI: 10.1073/pnas.1600672113. View

16.

Ding S, Cai Z, Du H, Wang H . Genome-Wide Analysis of TCP Family Genes in L. Identified a Role for in Drought Tolerance. Int J Mol Sci. 2019; 20(11). PMC: 6600213. DOI: 10.3390/ijms20112762. View

17.

Zhang H, Lang Z, Zhu J . Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol. 2018; 19(8):489-506. DOI: 10.1038/s41580-018-0016-z. View

18.

Welchen E, Garcia L, Mansilla N, Gonzalez D . Coordination of plant mitochondrial biogenesis: keeping pace with cellular requirements. Front Plant Sci. 2014; 4:551. PMC: 3884152. DOI: 10.3389/fpls.2013.00551. View

19.

Wijnen H, Young M . Interplay of circadian clocks and metabolic rhythms. Annu Rev Genet. 2006; 40:409-48. DOI: 10.1146/annurev.genet.40.110405.090603. View

20.

Liu N, Liu J, Li W, Pan Q, Liu J, Yang X . Intraspecific variation of residual heterozygosity and its utility for quantitative genetic studies in maize. BMC Plant Biol. 2018; 18(1):66. PMC: 5909218. DOI: 10.1186/s12870-018-1287-4. View