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Hybrid vigor or heterosis is a fascinating phenomenon with far-reaching impact on human health and agriculture. Heterosis refers to increased growth and fertility of the offspring that is superior to one or both parents, as seen in Arabidopsis and maize (or corn); all commercial corn grown in the U.S. is hybrid. The concept of heterosis extends beyond plants to include farm animals and humans. In humans, heterosis manifests in many ways, including improved stature, attractiveness, and intelligence. Heterozygote advantage, as observed in sickle cell anemia, shows heterozygote carriers having a selective advantage against certain diseases such as malaria. Conversely, inbreeding depression leads to diseases and low fertility because of reduced genetic diversity and unmasking of deleterious alleles. Since Charles Darwin systematically described heterosis in 1867, genetic models including dominance and overdominance have been debated over a century but cannot fully explain the basis of heterosis.
In A. thaliana, circadian regulators affect rhythms and period of the clock as well as its input and output pathways. At least ~10% of genes, including those involved in photosynthesis and starch metabolism, and up to 30% of transcriptome are regulated by the circadian rhythms. Moreover, day-length and circadian effects on transitory starch metabolism correlate with diurnal expression of these metabolic genes. Hence, maintaining circadian regulation increases CO2 fixation and growth, whereas disrupting circadian rhythms reduces fitness. Using Arabidopsis hybrids and allopolyploids as experimental systems, we are testing how and why circadian rhythms are altered to promote growth vigor and improve fitness.
We made seminal contributions to the understanding of molecular bases of hybrid vigor and inbreeding depression. Our studies have linked altered circadian rhythms with increased growth vigor in plant hybrids and allotetraploids. Hybridization induces epigenetic changes to alter clock gene expression waveforms of CCA1 and LHY and the reciprocal regulators TOC1 while to maintain the clock period, which in turn increase the expression of circadian output genes in photosynthetic and metabolic (starch) pathways, leading to growth vigor. The more starch accumulate during the day, the more it can be utilized and degraded at night to promote growth.
This breakthrough finding that linked altered circadian rhythms with hybrid vigor is provocative but logical because the clock regulates metabolism and physiology in plants and animals. mPer2-/- mice lack a glucocorticoid rhythm, while Clock-/- mutant mice are obese and have metabolic syndromes. In humans, energy intake and metabolism have a diurnal rhythm, and disruption of circadian rhythms leads to obesity and cardiovascular diseases.
The circadian clock also gates the timing of stress responses in the hybrids, which are normally repressed but activated under stress at specific times of the day. This timing mechanism helps balance defense and growth, enhancing hybrid performance under varying environmental conditions. Moreover, the circadian clock also influences ethylene production, a hormone that typically inhibits vegetative growth but promotes fruit maturation. In hybrids, ethylene response genes are downregulated during the day through a CCA1-mediated pathway and phytochrome interacting factors at night, thus promoting growth vigor. Circadian regulation of hybrid vigor is conserved across species. Hybrids in maize exhibit nonadditive expression patterns of key enzymes in photosynthetic and photorespiratory pathways, optimizing metabolic processes and enhancing overall plant growth.
We further identified reversible epigenetic modifications of TCP-target genes as a key factor in inbreeding depression in maize. This discovery adds another layer to understanding how genetic and epigenetic factors interplay to influence plant fitness. Our contributions have shifted the paradigm from traditional genetic models to a focus on the molecular and regulatory mechanisms underpinning hybrid vigor and inbreeding depression.
Our research provides new avenues for manipulating hybrid vigor to improve crop yields and resilience, including creating growth vigor in non-hybrid strains. Given that ~25% of global carbon emissions are captured by plant ecosystems as biomass and belowground soil-root organic matter, increasing plant biomass and shifting carbon flow towards roots and soil microbiomes provides a long-term solution to carbon sequestration and climate mitigation.
Five Selected Publications
- Ni, Z., Kim, E., Ha, M., Lackey, E., Liu, J., Zhang, Y., Sun, Q., and Chen, Z. J. (2009) Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids. Nature 457:327-331.
- Chen, Z. J. (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nature Reviews Genetics 14:471-482.
- Miller, M., Song, Q., Shi, X., Juenger, T. E., and Chen, Z. J. (2015) Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis. Nature Communications 6:7453.
- Li, Z., Zhu, A., Song, Q., Chen, H. Y., Harmon, F. G., Chen, Z. J. (2020) Temporal regulation of metabolome and proteome in photosynthetic and photorespiratory pathways contributes to maize heterosis. The Plant Cell 32:3706-3722.
- Han, T., Wang, F., Song, Q., Ye, W., Liu, T., Wang, L., Chen, Z. J. (2021) An epigenetic basis for inbreeding depression in maize. Science Advances 7(35):eabg5442.
