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.

Figure 1

Various light environments influence plant pigment accumulation and biomass in tomato seedlings. A Spectrum of different light qualities. B Representative images of tomato leaves cultured under white (W), red-white (R1W1 and R3W2), and red-white-blue (R1W1B0.5) light conditions. Scale bar = 2 cm. C–H ProtoIX (C), Mg-ProtoIX (D), Pchlide (E), chlorophyll (Chl; F), carotenoid (G), and anthocyanin (H) contents in tomato leaves at the five-leaf stage after transfer to various light conditions (W, R1W1, R3W2, and R1W1B0.5) for 15 days. I, J Fresh weight (I) and dry weight (J) of plants grown under various light conditions for 15 days. Values are means of three biological replicates (± standard deviation). Statistically significant differences between means are denoted by different letters.

Figure 2

Light quality regulates photosynthesis and electron transport rates in tomato plants. A–D Net photosynthetic rate (Pn; A), transpiration rate (Tr; B), intercellular CO₂ concentration (Ci; C), and stomatal conductance (Gs; D) in tomato leaves cultured under white (W), red-white (R1W1 and R3W2), and red-white-blue (R1W1B0.5) light conditions for 15 days. E–H Effective quantum yield of PSII [Y(II); E] and PSI [Y(I); F], and electron transport rates of PSII [ETR(II); G] and PSI [ETR(I); H] after tomato exposure to W, R1W1, R3W2, and R1W1B0.5 light treatments for 15 days. I, J NPQ (I) and 1−qP (J) after tomato exposure to W, R1W1, R3W2, and R1W1B0.5 light treatments for 15 days. Values are means of three biological replicates (± standard deviation). In A–D, statistically significant differences between means are denoted by different letters.

Figure 3

Light quality influences the photosynthetic capacity of tomato plants. A Light quality regulates electron absorption, transport, and energy distribution in the photosynthetic response. B Expression of LIGHT-HARVESTING COMPLEX B and A in leaves of tomato plants grown under white (W), red-white (R1W1 and R3W2), and red-white-blue (R1W1B0.5) light conditions for 3 days. C, D Performance for energy conservation from photons absorbed by PSII to reduction of intersystem electron acceptors (PI_ABS; C) and performance up to the PSI end electron acceptors (PI_total; D) in leaves of tomato plants grown under W, R1W1, R3W2, and R1W1B0.5 light conditions for 15 days. Values are means of three biological replicates (± standard deviation). Statistically significant differences between means are denoted by different letters in A, C, and D.

Figure 4

Light quality regulates fruit ripening and metabolism accumulation through an SlCYCB-dependent pathway. A Representative image of tomato fruits grown under white (W), red-white (R1W1 and R3W2), and red-white-blue (R1W1B0.5) light conditions for 10 days at the mature green stage. Scale bar = 2 cm. B–E Color index (a*/b*; B), fruit firmness (C), carotenoid content (D), and expression of SlCYCB gene (E) in tomato fruit after exposure to various light conditions for 10 days. F Representative image of tomato fruits in SlCYCB-silenced fruits (pTRV-SlCYCB) and WT (pTRV) fruits cultured under various light conditions for 5 days. Scale bar = 2 cm. G, H Color index (a*/b*; G) and lycopene contents (H) of pTRV-SlCYCB and pTRV in tomato fruit cultured for 5 days. Values are means of three biological replicates (± standard deviation). Statistically significant differences between means are denoted by different letters in bar graphs.

Figure 5

Disruption of SlCYCB reduces chlorophyll accumulation and photosynthesis rates in tomato plants under various light conditions. A Representative leaf images of SlCYCB-silenced plants (pTRV-SlCYCB) and WT (pTRV) cultured under white (W), red (R), and blue (B) light conditions for 15 days. Scale bar = 2 cm. B–D Contents of chlorophyll a (B) and b (C), and total chlorophyll (D) in pTRV-SlCYCB and pTRV plants cultured under W, B, and R light for 15 days. E–H Net photosynthetic rate (Pn; E), transpiration rate (Tr; F), intercellular CO₂ concentration (Ci; G), and stomatal conductance (Gs; H) in pTRV-SlCYCB and pTRV tomato plant leaves cultured under W, B, and R light for 15 days. Values are means of three biological replicates (± standard deviation). Statistically significant differences between means are denoted by different letters.

Figure 6

Disruption of SlCYCB reduces the effective quantum yield and electron transport rates of PSII and PSI. A, B Effective quantum yield of PSII [Y(II); A] and PSI [Y(I); B] in SlCYCB-silenced plants (pTRV-SlCYCB) and WT (pTRV) after exposure to white (W), red (R), and blue (B) light conditions for 15 days. C, D Electron transport rates of PSII [ETR(II); C] and PSI [ETR(I); D] in pTRV-SlCYCB and pTRV plants after exposure to white (W), red (R), and blue (B) light conditions for 15 days. Values are means of three biological replicates (± standard deviation).

Figure 7

Disruption of SlPHYB1 and SlCRY1 reduces chlorophyll accumulation, photosynthesis, and electron transport rates. A, B Representative tomato leaf images (A) and chlorophyll contents (B) of slphyb1cry1 mutant and WT plants cultured under white (W) and red-white-blue (R1W1B0.5) light conditions for 15 days. Scale bar = 2 cm. C–E Maximum quantum yield of PSII (Fv/Fm; C, D) and net photosynthetic rate (Pn; E) in slphyb1cry1 mutant and WT plants under W and R1W1B0.5 light conditions for 15 days.Scale bar = 2 cm. F, G Electron transport rates of PSII [ETR(II); F] and PSI [ETR(I); G] in slphyb1cry1 mutant and WT plants under W and R1W1B0.5 light conditions for 15 days. H Gene expression of SlLHCA, SlLHCB, and SlCYCB in leaves of slphyb1cry1 mutant and WT plants cultured under W and R1W1B0.5 light conditions for 3 days. Values are means of three biological replicates (± standard deviation). Statistically significant differences between means are denoted by different letters.

Figure 8

SlHY5 directly activates SlLHCA, SlLHCB, and SlCYCB to promote chlorophyll accumulation and photosynthesis. ASlHY5 gene expression in slphyb1cry1 mutant and WT plants grown under white (W) and red-white-blue (R1W1B0.5) light conditions for 3 days. B, C Chlorophyll contents (B) and net photosynthetic rate (Pn; C) in WT, SlHY5-overexpressing plants (SlHY5-OE), and slhy5 mutants cultured under R1W1B0.5 light conditions for 15 days. D The transcript levels of SlLHCA, SlLHCB, and SlCYCB in leaves of WT plants and SlHY5-OE and slhy5 mutants cultured under R1W1B0.5 light conditions for 3 days. E EMSA of SlHY5 associated with SlLHCA, SlLHCB, and SlCYCB. F, G Dual-luciferase assay for SlHY5 regulation of the expression of SlLHCA, SlLHCB, and SlCYCB. Values are means of three biological replicates (± standard deviation). Statistically significant differences between means are denoted by different letters.

Figure 9

A proposed model of light quality regulation of photosynthesis and fruit metabolism in tomato. Manipulation of light environments promotes the accumulation of chlorophyll, carotenoid, and anthocyanin, and enhances photosynthesis and electron transport rates by increasing the density of active reaction centers and the expression of LIGHT-HARVESTING COMPLEX B and A, resulting in increased plant biomass in tomato. In addition, R1W1B0.5 light induces fruit ripening and carotenoid accumulation by decreasing the expression of LYCOPENE β-CYCLASE (SlCYCB). In brief, R1W1B0.5 light noticeably promotes photosynthesis, biomass, and fruit quality through the photoreceptor (SlPHYB1 and SlCRY1)-SlHY5-SlLHCA/B/SlCYCB module in tomato.