Integrative physiological and transcriptome analyses elucidate the effect of shading during the grain-filling stage of wheat (Triticum aestivum) cv. ZY96-3
Tao Li A B # , Muhammad Arif A B # , Zhongni Wang C , Guanyin Shi A B , Lulwah Zeyad Aljumaiah D , Ling Xu A B , Mingjian Ren A B , Ruhong Xu A B * and Luhua Li
A B *
A
B
C
D
# These authors contributed equally to this paper
Handling Editor: Sajid Fiaz
Abstract
Shading plays an important role in determining nutrient content and yield fo wheat (Triticum aestivum). However, the genetic mechanism underlying the effects of shading treatment on grain filling remains unclear. Therefore, we performed phenotypic and transcriptome analyses on wheat cv. ZY96-3 during grain development under normal and shaded conditions. Shading resulted in a significant decrease in grain size and 1000-grain weight. Correlation analysis revealed the strong effect of shading on the mean and maximum grain-filling rate and secondary grain-filling parameters R2 and R3. And shading reduced starch content and starch-related enzyme activity (including granule-bound starch synthase and soluble starch synthase). Transcriptomic analyses showed that shading mainly affected pathways related to photosynthetic antenna proteins, carbon fixation in photosynthetic organisms, and starch and sucrose metabolism. Sixteen genes related to photosynthetic antenna protein and carbon fixation pathways were first upregulated and then downregulated; whereas all differentially expressed genes (PetC, Fd, LFNR1, LFNR2, PC, PsbO, PsaG, and PSB28) in the photosynthetic antenna protein pathway belonged to electron transport chain proteins. We found that shading treatment affects the physiological and molecular properties of grain development during the grain-filling stage. This study reveals new candidate genes (such as TaLFNR1-7A and TaFd-7A) for breeding wheat varieties with high photosynthetic efficiency in regions with insufficient light intensity.
Keywords: carbon fixation, differentially expressed genes, grain filling, photosynthesis, shading, transcriptomic analysis, wheat, yield.
References
Abdelrahman M, Burritt DJ, Gupta A, Tsujimoto H, Tran L-SP (2020) Heat stress effects on source-sink relationships and metabolome dynamics in wheat. Journal of Experimental Botany 71, 543-554.
| Crossref | Google Scholar |
Ali S, Xu Y, Ahmad I, Jia Q, Fangyuan H, Daur I, et al. (2018) The ridge furrow cropping technique indirectly improves seed filling endogenous hormonal changes and winter wheat production under simulated rainfall conditions. Agricultural Water Management 204, 138-148.
| Crossref | Google Scholar |
Arenas-Corraliza MG, Rolo V, López-Díaz ML, Moreno G (2019) Wheat and barley can increase grain yield in shade through acclimation of physiological and morphological traits in Mediterranean conditions. Scientific Reports 9, 9547.
| Crossref | Google Scholar |
Binkert M, Kozma-Bognár L, Terecskei K, De Veylder L, Nagy F, Ulm R (2014) UV-B-responsive association of the Arabidopsis bZIP transcription factor ELONGATED HYPOCOTYL5 with target genes, including its own promoter. The Plant Cell 26, 4200-4213.
| Crossref | Google Scholar | PubMed |
Cheng Y, Wang Y, Han Y, Li D, Zhang Z, Zhu X, et al. (2019) The stimulatory effects of nanochitin whisker on carbon and nitrogen metabolism and on the enhancement of grain yield and crude protein of winter wheat. Molecules 24, 1752.
| Crossref | Google Scholar |
Fan Y, Chen J, Wang Z, Tan T, Li S, Li J, et al. (2019) Soybean (Glycine max L. Merr.) seedlings response to shading: leaf structure, photosynthesis and proteomic analysis. BMC Plant Biology 19, 34.
| Crossref | Google Scholar |
Figueroa CM, Lunn JE, Iglesias AA (2021) Nucleotide-sugar metabolism in plants: the legacy of Luis F. Leloir. Journal of Experimental Botany 72, 4053-4067.
| Crossref | Google Scholar |
Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Molecular Plant 9, 1353-1365.
| Crossref | Google Scholar | PubMed |
Gao Y, An K, Guo W, Chen Y, Zhang R, Zhang X, et al. (2021) The endosperm-specific transcription factor TaNAC019 regulates glutenin and starch accumulation and its elite allele improves wheat grain quality. The Plant Cell 33, 603-622.
| Crossref | Google Scholar |
Geng J, Li L, Lv Q, Zhao Y, Liu Y, Zhang L, et al. (2017) TaGW2-6A allelic variation contributes to grain size possibly by regulating the expression of cytokinins and starch-related genes in wheat. Planta 246, 1153-1163.
| Crossref | Google Scholar |
Goss T, Hanke G (2014) The end of the line: can ferredoxin and ferredoxin NADP(H) oxidoreductase determine the fate of photosynthetic electrons? Current Protein & Peptide Science 15, 385-393.
| Crossref | Google Scholar |
Han W, Lin X, Wang D (2023) Uncovering the primary drivers of regional variability in the impact of climate change on wheat yields in china. Journal of Cleaner Production 421, 138479.
| Crossref | Google Scholar |
Hanke G, Mulo P (2013) Plant type ferredoxins and ferredoxin-dependent metabolism. Plant, Cell & Environment 36, 1071-1084.
| Crossref | Google Scholar | PubMed |
Hanke GT, Okutani S, Satomi Y, Takao T, Suzuki A, Hase T (2005) Multiple iso-proteins of FNR in Arabidopsis: evidence for different contributions to chloroplast function and nitrogen assimilation. Plant, Cell & Environment 28, 1146-1157.
| Crossref | Google Scholar |
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology 37, 907-915.
| Crossref | Google Scholar |
Kumar P, Madhawan A, Sharma A, Sharma V, Das D, Parveen A, et al. (2024) A sucrose non-fermenting-1-related protein kinase 1 gene from wheat, TaSnRK1α regulates starch biosynthesis by modulating AGPase activity. Plant Physiology and Biochemistry 207, 108407.
| Crossref | Google Scholar |
Li H, Tong Y, Li B, Jing R, Lu C, Li Z (2010a) Genetic analysis of tolerance to photo-oxidative stress induced by high light in winter wheat (Triticum aestivum L.). Journal of Genetics and Genomics 37, 399-412.
| Crossref | Google Scholar |
Li H, Jiang D, Wollenweber B, Dai T, Cao W (2010b) Effects of shading on morphology, physiology and grain yield of winter wheat. European Journal of Agronomy 33, 267-275.
| Crossref | Google Scholar |
Li H, Cai J, Jiang D, Liu F, Dai T, Cao W (2013) Carbohydrates accumulation and remobilization in wheat plants as influenced by combined waterlogging and shading stress during grain filling. Journal of Agronomy and Crop Science 199, 38-48.
| Crossref | Google Scholar |
Li H, Wang G, Zheng Q, Li B, Jing R, Li Z (2014) Genetic analysis of biomass and photosynthetic parameters in wheat grown in different light intensities. Journal of Integrative Plant Biology 56, 594-604.
| Crossref | Google Scholar |
Li Q, Zhong S, Sun S, Fatima SA, Zhang M, Chen W, et al. (2017) Differential effect of whole-ear shading after heading on the physiology, biochemistry and yield index of stay-green and non-stay-green wheat genotypes. PLoS ONE 12, e0171589.
| Crossref | Google Scholar |
Li X, Qian X, Lǚ X, Wang X, Ji N, Zhang M, et al. (2018) Upregulated structural and regulatory genes involved in anthocyanin biosynthesis for coloration of purple grains during the middle and late grain-filling stages. Plant Physiology and Biochemistry 130, 235-247.
| Crossref | Google Scholar |
Li W, Liu Y, Liu M, Zheng Q, Li B, Li Z, et al. (2019) Sugar accumulation is associated with leaf senescence induced by long-term high light in wheat. Plant Science 287, 110169.
| Crossref | Google Scholar |
Li L, Yang S, Wang Z, Ren M, An C, Xiong F, et al. (2023) Physiological and cytological analyses of the thousand-grain weight in ‘Zhongyan96-3’ wheat. Journal of Plant Growth Regulation 42, 2212-2220.
| Crossref | Google Scholar |
Liu X, Cai R, Li Y, Zhang M, Yang M, Zhang Y (2017) Starch component characteristics and physicochemical properties in wheat grains with different amylose contents in relation to low light after anthesis. Starch - Stärke 70, 1700050.
| Crossref | Google Scholar |
Liu H, Si X, Wang Z, Cao L, Gao L, Zhou X, et al. (2023a) TaTPP-7A positively feedback regulates grain filling and wheat grain yield through T6P-SnRK1 signalling pathway and sugar-ABA interaction. Plant Biotechnology Journal 21, 1159-1175.
| Crossref | Google Scholar |
Liu L, Wu F, Wang Y, Zhang T, Tang L, Yan C (2023b) Comparative transcriptome analyses revealed photosynthesis- and sucrose metabolism-related responses of endangered evergreen tree species Phoebe bournei (Hemsl.) Yang-Lauraceae to shade. Pakistan Journal of Botany 55, 2283-2293.
| Crossref | Google Scholar |
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15(12), 550.
| Crossref | Google Scholar |
Lv X, Zhang Y, Zhang Y, Fan S, Kong L (2020) Source-sink modifications affect leaf senescence and grain mass in wheat as revealed by proteomic analysis. BMC Plant Biology 20, 257.
| Crossref | Google Scholar |
Ma X, Ren X, Gao H, Wu X, Chen K, Khan R (2023) Proteomic, transcriptomic, biochemical, and physio-anatomical analyses provide insights into energy metabolism, light usage, and photosynthesis in cigar tobacco under different light intensities. Industrial Crops and Products 198, 116651.
| Crossref | Google Scholar |
Ma H, Yang Y, Wu D, Xiang G, Luo T, Huang X, et al. (2024a) Changes in free amino acid and protein polymerization in wheat caryopsis and endosperm during filling after shading. Frontiers in Plant Science 15, 1344972.
| Crossref | Google Scholar |
Ma H, Yang Y, Zhao J, Huang X, Yang H, Zheng T, et al. (2024b) Relationship between the baking quality of wheat (Triticum aestivum L.) and the protein composition and structure after shading. Food Chemistry 441, 138392.
| Crossref | Google Scholar |
Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21, 3787-3793.
| Crossref | Google Scholar |
Marchetti CF, Škrabišová M, Galuszka P, Novák O, Causin HF (2018) Blue light suppression alters cytokinin homeostasis in wheat leaves senescing under shading stress. Plant Physiology and Biochemistry 130, 647-657.
| Crossref | Google Scholar |
Martı́nez-Trujillo M, Chávez-Bárcenas T, Limones-Briones V, Simpson J, Herrera-Estrella L (2004) Functional analysis of the promoter of the rice sucrose phosphate synthase gene (sps1). Plant Science 166, 131-140.
| Crossref | Google Scholar |
Mastilović J, Živančev D, Lončar E, Malbaša R, Hristov N, Kevrešan Ž (2018) Effects of high temperatures and drought during anthesis and grain filling period on wheat processing quality and underlying gluten structural changes. Journal of the Science of Food and Agriculture 98, 2898-2907.
| Crossref | Google Scholar |
Milner MJ, Swarbreck SM, Craze M, Bowden S, Griffiths H, Bentley AR, et al. (2022) Over-expression of TaDWF4 increases wheat productivity under low and sufficient nitrogen through enhanced carbon assimilation. Communications Biology 5, 193.
| Crossref | Google Scholar |
Mu H, Jiang D, Wollenweber B, Dai T, Jing Q, Cao W (2010) Long-term low radiation decreases leaf photosynthesis, photochemical efficiency and grain yield in winter wheat. Journal of Agronomy and Crop Science 196, 38-47.
| Crossref | Google Scholar |
Nan X, Li W, Shao M, Cui Z, Wang H, Huo J, et al. (2024) Shading treatment reduces grape sugar content by suppressing photosynthesis-antenna protein pathway gene expression in grape berries. International Journal of Molecular Sciences 25, 5029.
| Crossref | Google Scholar |
Nehe AS, Misra S, Murchie EH, Chinnathambi K, Singh TB, Foulkes MJ (2020) Nitrogen partitioning and remobilization in relation to leaf senescence, grain yield and protein concentration in Indian wheat cultivars. Field Crops Research 251, 107778.
| Crossref | Google Scholar |
Paulišić S, Qin W, Arora Verasztó H, Then C, Alary B, Nogue F, et al. (2021) Adjustment of the PIF7-HFR1 transcriptional module activity controls plant shade adaptation. The EMBO Journal 40, e104273.
| Crossref | Google Scholar |
Qiao X, Sai L, Chen X, Xue L, Lei J (2019) Impact of fruit-tree shade intensity on the growth, yield, and quality of intercropped wheat. PLoS ONE 14, e0203238.
| Crossref | Google Scholar |
Rharrabti Y, Elhani S, Martos-Núñez V, García del Moral LF (2001) Protein and lysine content, grain yield, and other technological traits in durum wheat under Mediterranean conditions. Journal of Agricultural and Food Chemistry 49, 3802-3807.
| Crossref | Google Scholar |
Shi Y, Chen J, Hou X (2020) Similarities and differences of photosynthesis establishment related mrnas and novel lncRNAs in early seedlings (coleoptile/cotyledon vs. true leaf) of rice and Arabidopsis. Frontiers in Genetics 11, 565006.
| Crossref | Google Scholar |
Solis-Badillo E, Agama-Acevedo E, Tiessen A, Lopez Valenzuela JA, Bello-Perez A (2020) ADP-glucose pyrophosphorylase is located in the plastid and cytosol in the pulp of tropical banana fruit (Musa acuminata). Plant Foods for Human Nutrition 75, 76-82.
| Crossref | Google Scholar |
Stein O, Granot D (2019) An overview of sucrose synthases in plants. Frontiers in Plant Science 10, 95.
| Crossref | Google Scholar |
Sun G, Yang L, Zhan W, Chen S, Song M, Wang L, et al. (2022) HFR1, a bHLH transcriptional regulator from arabidopsis thaliana, improves grain yield, shade and osmotic stress tolerances in common wheat. International Journal of Molecular Sciences 23, 12057.
| Crossref | Google Scholar |
Suzuki Y, Makino A (2012) Availability of rubisco small subunit up-regulates the transcript levels of large subunit for stoichiometric assembly of its holoenzyme in rice. Plant Physiology 160, 533-540.
| Crossref | Google Scholar |
Wang Y, Zhang Z, Liang Y, Han Y, Han Y, Tan J (2020) High potassium application rate increased grain yield of shading-stressed winter wheat by improving photosynthesis and photosynthate translocation. Frontiers in Plant Science 11, 134.
| Crossref | Google Scholar |
Wang J, Shi K, Lu W, Lu D (2021a) Effects of post-silking shading stress on enzymatic activities and phytohormone contents during grain development in spring maize. Journal of Plant Growth Regulation 40, 1060-1073.
| Crossref | Google Scholar |
Wang Z, Ma H, Zhang M, Wang Z, Tian Y, Li W, et al. (2021b) Transcriptional response of Asarum heterotropoides Fr. Schmidt var. mandshuricum (Maxim.) Kitag. leaves grown under full and partial daylight conditions. BMC Genomics 22, 16.
| Crossref | Google Scholar |
Wang X, Liu Y, Hao C, Li T, Majeed U, Liu H, et al. (2023) Wheat NAC-A18 regulates grain starch and storage proteins synthesis and affects grain weight. Theoretical and Applied Genetics 136, 123.
| Crossref | Google Scholar |
WenminQin , Wang L, Gueymard C, Bilal M, Lin A, Wei J, et al. (2020) Constructing a gridded direct normal irradiance dataset in china during 1981–2014. Renewable and Sustainable Energy Reviews 131, 110004.
| Crossref | Google Scholar |
Wu X, Tang Y, Li C, Wu C (2018) Characterization of the rate and duration of grain filling in wheat in southwestern China. Plant Production Science 21(4), 358-369.
| Crossref | Google Scholar |
Xie D, Hao M, Zhao L, Chen X, Chen X, Jiang B, et al. (2023) Transcriptomic analysis provides insight into the genetic regulation of shade avoidance in Aegilops tauschii. BMC Plant Biology 23, 336.
| Crossref | Google Scholar |
Yang X, Asseng S, Wong MTF, Yu Q, Li J, Liu E (2013) Quantifying the interactive impacts of global dimming and warming on wheat yield and water use in China. Agricultural and Forest Meteorology 182-183, 342-351.
| Crossref | Google Scholar |
Yang H, Dong B, Wang Y, Qiao Y, Shi C, Jin L, et al. (2020) Photosynthetic base of reduced grain yield by shading stress during the early reproductive stage of two wheat cultivars. Scientific Reports 10, 14353.
| Crossref | Google Scholar |
Yang H, Zhao J, Ma H, Shi Z, Huang X, Fan G (2023a) Shading affects the starch structure and digestibility of wheat by regulating the photosynthetic light response of flag leaves. International Journal of Biological Macromolecules 236, 123972.
| Crossref | Google Scholar |
Yang H, Li Y, Zhao J, Chen Z, Huang X, Fan G (2023b) Regulating the composition and secondary structure of wheat protein through canopy shading to improve dough performance and nutritional index. Food Research International 173, 113399.
| Crossref | Google Scholar |
Yang S, Zhang Z, Chen W, Liang C, Li X, Liu Z, et al. (2023c) Fine-mapping and transcriptome analysis of the photosensitive leaf-yellowing gene CaLY1 in pepper (Capsicum annuum L.). Horticultural Plant Journal 9, 122-132.
| Crossref | Google Scholar |
Yi Z, Cui J, Fu Y, Liu H (2020) Effect of different light intensity on physiology, antioxidant capacity and photosynthetic characteristics on wheat seedlings under high CO2 concentration in a closed artificial ecosystem. Photosynthesis Research 144, 23-34.
| Crossref | Google Scholar |
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biology 11, R14.
| Crossref | Google Scholar |
Zhang W, Han S, Wang M, Aubrey A, Pan M, Aaasimu A, et al. (2021) Effects of fruit tree canopy shading on grain filling of intercropping winter wheat. Chinese Journal of Applied Ecology 32, 2458-2468.
| Crossref | Google Scholar |
Zhang W, Wang B, Zhang A, Zhou Q, Li Y, Li L, et al. (2022) Exogenous 6-benzylaminopurine enhances waterlogging and shading tolerance after anthesis by improving grain starch accumulation and grain filling. Frontiers in Plant Science 13, 1003920.
| Crossref | Google Scholar |
Zhang Q, Jin M, An D, Ahmed Z, Qi Y, Xu B (2023) Modelling dried noodle quality: contribution of starch and protein physicochemical properties of 32 wheat cultivars. Food Research International 174, 113501.
| Crossref | Google Scholar |
Zheng X, Yu Z, Yu F, Shi Y (2022) Grain-filling characteristics and yield formation of wheat in two different soil fertility fields in the Huang-Huai-Hai Plain. Frontiers in Plant Science 13, 932821.
| Crossref | Google Scholar |
Zhu T, Jackson DS, Wehling RL, Geera B (2008) Comparison of amylose determination methods and the development of a dual wavelength iodine binding technique. Cereal Chemistry 85, 51-58.
| Crossref | Google Scholar |
Zi Y, Ding J, Song J, Humphreys G, Peng Y, Li C, et al. (2018) Grain yield, starch content and activities of key enzymes of waxy and non-waxy wheat (Triticum aestivum L.). Scientific Reports 8, 4548.
| Crossref | Google Scholar |
Zörb C, Ludewig U, Hawkesford MJ (2018) Perspective on wheat yield and quality with reduced nitrogen supply. Trends in Plant Science 23, 1029-1037.
| Crossref | Google Scholar |
