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. 2020 Apr 1;3(1):151.
doi: 10.1038/s42003-020-0887-3.

Maize GOLDEN2-LIKE Genes Enhance Biomass and Grain Yields in Rice by Improving Photosynthesis and Reducing Photoinhibition

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Free PMC article

Maize GOLDEN2-LIKE Genes Enhance Biomass and Grain Yields in Rice by Improving Photosynthesis and Reducing Photoinhibition

Xia Li et al. Commun Biol. .
Free PMC article

Abstract

Photosynthetic efficiency is a major target for improvement of crop yield potential under agricultural field conditions. Inefficiencies can occur in many steps of the photosynthetic process, from chloroplast biogenesis to functioning of the light harvesting and carbon fixation reactions. Nuclear-encoded GOLDEN2-LIKE (GLK) transcription factors regulate some of the earliest steps by activating target genes encoding chloroplast-localized and photosynthesis-related proteins. Here we show that constitutive expression of maize GLK genes in rice leads to enhanced levels of chlorophylls and pigment-protein antenna complexes, and that these increases lead to improved light harvesting efficiency via photosystem II in field-grown plants. Increased levels of xanthophylls further buffer the negative effects of photoinhibition under high or fluctuating light conditions by facilitating greater dissipation of excess absorbed energy as heat. Significantly, the enhanced photosynthetic capacity of field-grown transgenic plants resulted in increased carbohydrate levels and a 30-40% increase in both vegetative biomass and grain yield.

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. ZmUBIpro:ZmGLK1 and ZmUBIpro:ZmG2 transgenic lines exhibit higher rates of photosynthesis than wild-type plants when grown in the field.
a Pigment content of flag leaves in WT and transgenic lines at the heading stage in the field in Beijing, 2018 (n = 6 biological replicates); bd light response curve of net photosynthesis fitted by the FvCB model (b), stomatal conductance (c), and intercellular CO2 concentration (Ci) (d) generated at 30 °C under normal air conditions in the field in Beijing, 2018 (n = 4 biological replicates). e Apparent quantum yield generated from fitted light response curves. Data are mean ± SE (n = 4 biological replicates). f CO2 response curve of net photosynthesis generated at 1200 µmol m−2 s−1 PPFD and 30 °C in the field in Beijing, 2019. Data are mean ± SE (n = 3 biological replicates). Each dot represents a biological replicate. *P < 0.05, **P < 0.01 compared with WT according to a two-tailed Student’s t test.
Fig. 2
Fig. 2. Elevated levels of D1 protein in ZmUBIpro:ZmGLK1 and ZmUBIpro:ZmG2 transgenic lines lead to better resistance to photoinhibition than wild-type plants in fluctuating light conditions.
af Non-photochemical quenching (NPQ) (a, b), quantum efficiency of photosystem II (ΦPSII) (c, d), and maximal PSII quantum efficiency (Fv/Fm) (e, f) under steady-state light (a, c, e) and after 3 days of treatment of fluctuating light (b, d, f) in WT and transgenic lines. Data are mean ± SE (n = 4 biological replicates), each dot represents a biological replicate. Different letters indicate a significant difference as determined by a one-way ANOVA test (P < 0.05). gj Photoinhibition of PSII and recovery kinetics in WT and transgenic lines, including maximal PSII quantum efficiency (Fv/Fm) measured in detached leaves soaked in H2O under high light conditions (g); Fv/Fm measured in detached leaves soaked in lincomycin under high light conditions (h); recovery of Fv/Fm after photoinhibition in H2O (i) and 1 mM lincomycin (j). Data are mean ± SE (n = 4 biological replicates). *P < 0.05, **P < 0.01 compared with WT according to a two-tailed Student’s t test. k Immunoblot analysis of D1 protein in extracts from detached leaves of WT and transgenic lines before and after a 4-h exposure to high light (HL) in the presence (Lin) or absence (H2O) of lincomycin. The Rubisco large subunit (LSU) was used as a loading control. The numbers below the gel lanes represent the relative protein level, which was quantified from the band intensity using the ImageJ software, and normalized relative to WT.
Fig. 3
Fig. 3. Diurnal variation of photosynthetic parameters and xanthophyll pigments.
a, b Diurnal change in Fv/Fm (a) and NPQ (b) values of flag leaves at the heading stage in the field in Beijing, 2018. Measurements were performed using a FluorPen. PPFD at each time point was 800, 1500, 2000, 900, and 350 µmol m−2 s−1, respectively. Data are mean ± SE (n = 4 biological replicates). c, d Diurnal curves of photosynthesis (c) and stomatal conductance (d) measured using a LICOR-6400 XT in the field from 9 a.m. to 5 p.m. in Hainan, 2019. PPFD at each time point was 600, 1200, 1500, 900, and 300 µmol m−2 s−1, respectively. All measurements were conducted with at least four biological replicates. Data are mean ± SE. e, f Diurnal change in zeaxanthin (e) and lutein (f) content. g Diurnal change in total content of xanthophyll pigments (V + A + Z). h Diurnal change in de-epoxidation state of the xanthophyll cycle calculated as the ratio (A + Z)/(V + A + Z)%. All pigments were measured in flag leaves sampled at the heading stage at 8 a.m., 12 a.m., and 6 p.m. from the field experiment in Beijing, 2019. Data are mean ± SE (n = 3 biological replicates). *P < 0.05, **P < 0.01 compared with WT according to a two-tailed Student’s t test.
Fig. 4
Fig. 4. Leaves of ZmUBIpro:ZmG2 transgenic plants accumulate significantly higher levels of starch and sugars than wild-type plants.
ad Starch (a), sucrose (b), glucose (c), and fructose (d) levels measured in flag leaves at the heading stage at 7 a.m., 12 a.m., and 7 p.m. in the field experiment in Hainan, 2019. Data are mean ± SE (n = 6 biological replicates), each dot represents a biological replicate. *P < 0.05, **P < 0.01 compared with WT according to two-tailed Student’s t test. e Hierarchical cluster analysis (HCA) of 95 primary metabolites in flag leaves at the heading stage in the field experiment in Beijing, 2018. Metabolite content is presented as median-centered averages with six biological replicates each. Red and blue colors indicate high and low content, respectively.
Fig. 5
Fig. 5. Increased vegetative biomass in ZmUBIpro:ZmGLK1 and ZmUBIpro:ZmG2 transgenic lines grown in Beijing and Hainan.
af Phenotypic parameters measured in the field experiment in Beijing, May 2018 to September 2018. All data were calculated from at least 20 independent rice plants. Data are mean ± SE. gl Phenotypic parameters measured in the field experiment in Hainan, December 2017 to April 2018. g, h, l were calculated from at least 20 independent rice plants. i, j, k were calculated from at least five independent rice plants. CK = null segregants isolated from selfed heterozygous transgenic plants. Box and whisker plots show median (line) and outliers (black dots (•)). *P < 0.05, **P < 0.01 compared with WT according to a two-tailed Student’s t test.
Fig. 6
Fig. 6. Enhanced grain yield in ZmUBIpro:ZmGLK1 and ZmUBIpro:ZmG2 transgenic lines in Beijing and Hainan.
ae Yield parameters obtained from the field experiment in Beijing, May 2018 to September 2018. fj Yield parameters obtained from the field experiment in Hainan, December 2017 to April 2018. All data except e and j were calculated from at least 20 independent rice plants. Seed yield per plot (e, j) was calculated from 30 independent rice plants within a plot and three plots that were placed randomly in the field. CK = null segregants isolated from selfed heterozygous transgenic plants. Box and whisker plots show median (line) and outliers (black dots (•)). In e, j, data are mean ± SE (n = 3 replicates). *P < 0.05, **P < 0.01 compared with WT according to a two-tailed Student’s t test. k, l Comparison of single panicle (k) and seed yield per plant (l) of WT and transgenic plants from the field experiment in Hainan, December 2017 to April 2018. Scale bars = 5 cm.

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