Qingxin Song, Atsumi Ando, Dongqing Xu, Lei Fang, Tianzhen Zhang, Enamul Huq, Hong Qiao, Xing Wang Deng, and Z. Jeffrey Chen

PNAS May 22, 2018. 115 (21) 5606-5611;

Significance

Heterosis is a fundamental biological phenomenon and important to crop and animal production. However, molecular mechanisms for heterosis remain elusive. Ethylene promotes fruit ripening but inhibits vegetative growth. Here we report that diurnal down-regulation of ethylene biosynthesis genes in Arabidopsis thaliana F1 hybrids corresponds to the decrease of ethylene production and biomass heterosis. Expression of ACS genes is diurnally and indirectly regulated by CCA1 during the day and directly regulated by PIF5 at night. Disruption of ethylene biosynthesis or signaling transduction leads to higher biomass, while application of exogenous ethylene reduced growth vigor, further validating the negative roles of ethylene in biomass heterosis. Thus, ethylene can integrate circadian rhythms and light signaling to regulate growth vigor in plant hybrids.

Abstract

Heterosis is widely applied in agriculture; however, the underlying molecular mechanisms for superior performance are not well understood. Ethylene biosynthesis and signaling genes are shown to be down-regulated in Arabidopsis interspecific hybrids. Ethylene is a plant hormone that promotes fruit ripening and maturation but inhibits hypocotyl elongation. Here we report that application of exogenous ethylene could eliminate biomass vigor in Arabidopsis thaliana F1 hybrids, suggesting a negative role of ethylene in heterosis. Ethylene biosynthesis is mediated by the rate-limiting enzyme, 1-aminocyclopropane-1-carboxylate synthase (ACS). Down-regulation of ACS genes led to the decrease of ethylene production, which was associated with the high-vigor F1 hybrids, but not with the low-vigor ones. At the mechanistic level, expression of ACS genes was down-regulated diurnally and indirectly by Circadian Clock Associated 1 (CCA1) during the day and directly by Phyotochrome-Interacting Factor 5 (PIF5) at night. Consistent with the negative role of ethylene in plant growth, biomass vigor was higher in the acs mutants than in wild-type plants, while increasing endogenous ethylene production in the hybridizing parents reduced growth vigor in the hybrids. Thus, integrating circadian rhythms and light signaling into ethylene production is another regulatory module of complex biological networks, leading to biomass heterosis in plants.

See http://www.pnas.org/content/115/21/5606

Figure 1: Ethylene biosynthesis is down-regulated in Arabidopsis hybrids. (A) Representative images of seedlings of Col-0, C24, reciprocal F1 hybrids (ColXC24 and C24XCol) with or without ACC treatments. (Scale bar, 1 cm.) (B) Quantitative analysis of rosette diameter in A. Double asterisks indicate statistical significance levels at P < 0.01 compared with the midparent value (MPV). (C) Relative expression levels (R.E.L.) of ACS genes at ZT0 in Col-0, C24, and F1 hybrid (ColXC24). Asterisks indicate down-regulation in the hybrids at the statistically significant level (P < 0.05) relative to MPV. (D) R.E.L. of ERF1A and ERF73 as the materials used in C. (E) Ethylene production in F1 and F1r hybrids and their parents. (F) R.E.L. of ACS genes in hybrid (ColXLer).