Light quality regulates plant biomass and fruit quality through a photoreceptor-dependent HY5-LHC/CYCB module in tomato

Abstract

Increasing photosynthesis and light capture offers possibilities for improving crop yield and provides a sustainable way to meet the increasing global demand for food. However, the poor light transmittance of transparent plastic films and shade avoidance at high planting density seriously reduce photosynthesis and alter fruit quality in vegetable crops, and therefore it is important to investigate the mechanisms of light signaling regulation of photosynthesis and metabolism in tomato (Solanum lycopersicum). Here, a combination of red, blue, and white (R1W1B0.5) light promoted the accumulation of chlorophyll, carotenoid, and anthocyanin, and enhanced photosynthesis and electron transport rates by increasing the density of active reaction centers and the expression of the genes LIGHT-HARVESTING COMPLEX B (SlLHCB) and A (SlLHCA), resulting in increased plant biomass. In addition, R1W1B0.5 light induced carotenoid accumulation and fruit ripening by decreasing the expression of LYCOPENE β-CYCLASE (SlCYCB). Disruption of SlCYCB largely induced fruit lycopene accumulation, and reduced chlorophyll content and photosynthesis in leaves under red, blue, and white light. Molecular studies showed that ELONGATED HYPOCOTYL 5 (SlHY5) directly activated SlCYCB, SlLHCB, and SlLHCA expression to enhance chlorophyll accumulation and photosynthesis. Furthermore, R1W1B0.5 light-induced chlorophyll accumulation, photosynthesis, and SlHY5 expression were largely decreased in the slphyb1cry1 mutant. Collectively, R1W1B0.5 light noticeably promoted photosynthesis, biomass, and fruit quality through the photoreceptor (SlPHYB1 and SlCRY1)-SlHY5- SlLHCA/B/SlCYCB module in tomato. Thus, the manipulation of light environments in protected agriculture is a crucial tool to regulate the two vital agronomic traits related to crop production efficiency and fruit nutritional quality in tomato.

Acknowledgements

We thank the Tomato Genetics Resource Center (http://tgrc.ucdavis.edu) for offering slphyb1cry1 mutant, ‘Moneymaker’, and ‘Ailsa Craig’ seeds. This work was funded by the National Natural Science Foundation of China (32122081, 32272698), the National Key Research and Development Program of China (2023YFF1002000), the Natural Science Foundation of Liaoning Province for Excellent Youth (2022-YQ-18), the National Key Research and Development Program of China (2019YFD1000300), the China Agriculture Research System (CARS-23), the National Natural Science Foundation of China (31801904, 31991184), the Liao Ning Revitalization Talents Program (XLYC1807020), the Young and Middle-aged Science and Technology Innovation Talent Support Program in Shenyang (RC200449), the Ministry of Science and Technology of the People’s Republic of China (DL2022026004L), and the Innovative Research Team (Science and Technology) in University of Henan Province (23IRTSTHN024).

Author contributions

T.L. and F.W. conceived and planned the research. J.Y., J.L., S.Y., C.J., Y.L., N.Z., Y.Z., X.S., K.Z., Y.P., X.W., and X.B. conducted the experiments. J.Y., Z.S., X.S., M.Q., S.M., C.T., T.L., Y.L., and F.W. analyzed the data. J.Y. and F.W. wrote the article. F.W., T.L., and G.A. revised the article. All authors read and approved the ultimate manuscript.

Data availability

All relevant data in this study are provided in the article and its supplementary files. All data and material reported in this manuscript are available from the corresponding author upon request.

Conflict of interest

The authors declare that they have no competing interest.

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