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Journal of Integrative Agriculture  2026, Vol. 25 Issue (2): 648-658    DOI: 10.1016/j.jia.2024.07.032
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Delayed photosynthesis response causes carbon assimilation reduction in soybean under fluctuating light

Jing Gao*, Shenglan Li*, Yi Lei, Qi Wang, Zili Ning, Zhaohong Lu, Xianming Tan, Mei Xu, Feng Yang#, Wenyu Yang

College of Agronomy, Sichuan Agricultural University/Sichuan Engineering Research Center for Crop Strip Intercropping System/Key Laboratory of Crop Ecophysiology and Farming System in Southwest, Ministry of Agriculture and Rural Affairs, Chengdu 611130, China
 Highlights 
● Soybeans grown under conditions of fluctuating light exhibit characteristics reminiscent of those adapted to low-light, including decreases in dry matter mass, leaf thinning, specific leaf weight, and chlorophyll (Chl) a/Chl b levels.
● The inhibitory impact of fluctuating light conditions on the growth of soybean plants arises from a decrease in carbon assimilation.  However, this is not attributed to acclimation to low-light periods, as the photosynthetic capacity remains unaffected by fluctuating light.
● The decrease in carbon assimilation is ascribed to a delayed photosynthetic response to fluctuations in light intensity.  When transitioning from low- to high-light, the gradual rate of stomatal opening limits carbon supply.  Moreover, upon returning to low-light, the gradual relaxation of photoprotection hinders light utilization efficiency.
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摘要  
田间生长的植物的光环境是高度动态的,不同物种对波动光(FL)的适应机制各异。大豆(Glycine max (L.) Merr.)在如何整合多种生理变化以适应FL方面仍存在不明确之处。本研究分析了在强弱光交替条件下大豆的光合气体交换参数和叶绿素(Chl)a荧光参数的变化,评估了FL条件对大豆形态和光合特性的影响。结果显示,FL处理下生长的大豆具有较低的干物质质量、小而薄的叶片和低的Chl a/Chl b,这些特征类似于在弱光环境中生长的大豆。然而,光合气体交换速率和光合能力保持恒定,与弱光处理有所不同。大豆对波动光和弱光的适应过程存在显著差异。相关性分析显示,在FL条件下,碳同化的降低主要由两个方面导致:由弱光过渡为强光时气孔导度增加缓慢以及再次转入弱光后非光化学猝灭的缓慢弛豫。因此,FL条件下碳同化的下降不能简单归因于弱光阶段的适应,而是由于光合作用的延迟响应造成的。


Abstract  

Plants encounter dynamic light environments in natural field conditions, and species differ in their physiological and biochemical mechanisms for acclimating to fluctuating light (FL).  The manner in which soybean (Glycine max (L.) Merr.) coordinates multiple physiological adjustments to FL remains poorly understood.  This study assessed the effects of FL on soybean morphology and photosynthetic traits by examining changes in photosynthetic gas exchange parameters and chlorophyll (Chl) a fluorescence under alternating high- and low-light conditions.  Results indicated that soybeans exposed to FL exhibited reduced dry matter accumulation, smaller and thinner leaves, and a lower Chl a/Chl b levels - characteristics typically associated with plants grown under continuous low-light.  Despite these morphological similarities, their photosynthetic gas exchange rates and photosynthetic capacity were maintained at levels comparable to those under steady high light, unlike plants grown under constant low-light.  Thus, acclimation to FL is distinct from adaptation to sustained low-light conditions.  Correlation analyses revealed that the decline in carbon assimilation under FL primarily stemmed from two factors: the slow recovery of stomatal conductance upon transition to high light and the delayed relaxation of nonphotochemical quenching when light intensity decreased.  Therefore, the reduction in carbon assimilation under FL cannot be attributed to low-light phase adjustments but rather reflects a lag in photosynthetic responsiveness to changing light conditions.

Keywords:  soybean       fluctuating light        CO2 assimilation        dynamic photosynthesis        photosynthetic limitation        stomatal opening        non-photochemical quenching  
Received: 11 March 2024   Accepted: 18 June 2024 Online: 22 July 2024  
Fund: 
This research was supported by the National Key Research and Development Program of China (2023YFF1001504), the National Natural Science Foundation of China (32071963), the National Key Research and Development Program of China (2022YFD2300902), the Guangxi Key Research and Development Program of China (GuikeAB23026107), and the Chengdu Science and Technology Project, China (2023-YF08-00003-SN).
About author:  Jing Gao, E-mail: 2020201020@stu.sicau.edu.cn; Shenglan Li, E-mail: lishenglan@stu.sicau.edu.cn; #Correspondence Feng Yang, E-mail: f.yang@sicau.edu.cn * These authors contributed equally to this study.

Cite this article: 

Jing Gao, Shenglan Li, Yi Lei, Qi Wang, Zili Ning, Zhaohong Lu, Xianming Tan, Mei Xu, Feng Yang, Wenyu Yang. 2026. Delayed photosynthesis response causes carbon assimilation reduction in soybean under fluctuating light. Journal of Integrative Agriculture, 25(2): 648-658.

Acevedo S L G, Coe R, Wang Y, Kromdijk J, Quick W P, Long S P. 2020. Variation in photosynthetic induction between rice accessions and its potential for improving productivity. New Phytologist, 227, 1097–1108.

Acevedo S L G, Coe R, Quick W P, Long S P. 2021. Variation between rice accessions in photosynthetic induction in flag leaves and underlying mechanisms. Journal of Experimental Botany, 72, 1282–1294.

Albanese P, Manfredi M, Re A, Marengo E, Saracco G, Pagliano C. 2018. Thylakoid proteome modulation in pea plants grown at different irradiances: quantitative proteomic profiling in a non-model organism aided by transcriptomic data integration. Plant Journal, 96, 786–800.

Bassi R, Dall’Osto L. 2021. Dissipation of light energy absorbed in excess: the molecular mechanisms. Annual Review of Plant Biology, 72, 47–76.

Blom T J, Zheng Y. 2009. The response of plant growth and leaf gas exchange to the speed of lamp movement in a greenhouse. Scientia Horticulturae, 119, 188–192.

Deans R M, Brodribb T J, Busch F A, Farquhar G D. 2019. Plant water-use strategy mediates stomatal effects on the light induction of photosynthesis. New Phytologist, 222, 382–395.

Duursma R A. 2015. Plantecophys - An R package for analysing and modelling leaf gas exchange data. PLoS ONE, 10, e0143346.

Evans J R, Poorter H. 2001. Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell and Environment, 8, 755–767.

Eyland D, van Wesemael J, Lawson T, Carpentier S. 2021. The impact of slow stomatal kinetics on photosynthesis and water use efficiency under fluctuating light. Plant Physiology, 186, 998–1012.

Gao J, Chen J, Lei Y, Wang Q, Zou J, Ning Z, Tan X, Yang F, Yang W. 2023. Functional consequences of light intensity on soybean leaf hydraulic conductance: coordinated variations in leaf venation architecture and mesophyll structure. Environmental and Experimental Botany, 210, 105301.

Garcia-Molina A, Leister D. 2020. Accelerated relaxation of photoprotection impairs biomass accumulation in arabidopsis. Nature Plants, 6, 9–12.

Givnish T J. 1988. Adaptation to sun and shade: A whole-plant perspective. Functional Plant Biology, 2, 63–92.

Greer D H. 2015. Seasonal changes in the photosynthetic response to CO2 and temperature in apple (Malus domestica cv. ‘red gala’) leaves during a growing season with a high temperature event. Functional Plant Biology, 42, 309–324.

Han J, Lei Z, Zhang Y, Yi X, Zhang W, Zhang Y. 2018. Drought-introduced variability of mesophyll conductance in gossypium and its relationship with leaf anatomy. Physiologia Plantarum, 166, 873–887.

Harley P C, Loreto F, Di Marco G, Sharkey T D. 1992. Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiology, 98, 1429–1436.

Herrmann H A, Schwartz J M, Johnson G N. 2020. From empirical to theoretical models of light response curves - linking photosynthetic and metabolic acclimation. Photosynthesis Research, 145, 5–14.

Hu W, Lu Z, Gu H, Ye X, Li X, Cong R, Ren T, Lu J. 2022. Potassium availability influences the mesophyll structure to coordinate the conductance of CO2 and H2O during leaf expansion. Plant Cell and Environment, 45, 2987–3000.

Huang G, Shu Y, Peng S, Li Y. 2022. Leaf photosynthesis is positively correlated with xylem and phloem areas in leaf veins in rice (Oryza sativa) plants. Annals of Botany, 129, 619–631.

Huber M, Nieuwendijk N M, Pantazopoulou C K, Pierik R. 2021. Light signalling shapes plant-plant interactions in dense canopies. Plant Cell and Environment, 44, 1014–1029.

Jiang C, Wang X, Gao H, Shi L, Chow W S. 2011. Systemic regulation of leaf anatomical structure, photosynthetic performance, and high-light tolerance in sorghum. Plant Physiology, 155, 1416–1424.

Kaiser E, Morales A, Harbinson J, Heuvelink E, Marcelis L. 2020. High stomatal conductance in the tomato flacca mutant allows for faster photosynthetic induction. Frontiers in Plant Science, 11, 1317.

Karpinski S, Szechynska-Hebda M, Wituszynska W, Burdiak P. 2013. Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell and Environment, 36, 736–744.

Kimura H, Hashimoto-Sugimoto M, Iba K, Terashima I, Yamori W. 2020. Improved stomatal opening enhances photosynthetic rate and biomass production in fluctuating light. Journal of Experimental Botany, 71, 2339–2350.

Kromdijk J, Glowacka K, Leonelli L, Gabilly S T, Iwai M, Niyogi K K, Long S P. 2016. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science, 354, 857–861.

Lawson T, Blatt M R. 2014. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiology, 164, 1556–1570.

Lehretz G G, Schneider A, Leister D, Sonnewald U. 2022. High non-photochemical quenching of vpz transgenic potato plants limits CO2 assimilation under high light conditions and reduces tuber yield under fluctuating light. Journal of Integrative Plant Biology, 64, 1821–1832.

Liu T, Barbour M M, Yu D, Rao S, Song X. 2022. Mesophyll conductance exerts a significant limitation on photosynthesis during light induction. New Phytologist, 233, 360–372.

Matsubara S. 2018. Growing plants in fluctuating environments: why bother? Journal of Experimental Botany, 69, 4651–4654.

Matthews J, Vialet-Chabrand S, Lawson T. 2018. Acclimation to fluctuating light impacts the rapidity of response and diurnal rhythm of stomatal conductance. Plant Physiology, 176, 1939–1951.

Mcausland L, Vialet-Chabrand S, Davey P, Baker N R, Brendel O, Lawson T. 2016. Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytologist, 211, 1209–1220.

Morales A, Kaiser E. 2020. Photosynthetic acclimation to fluctuating irradiance in plants. Frontiers in Plant Science, 11, 268.

Nunes T, Zhang D, Raissig M T. 2020. Form, development and function of grass stomata. Plant Journal, 101, 780–799.

Pao Y C, Stutzel H, Chen T W. 2019. A mechanistic view of the reduction in photosynthetic protein abundance under diurnal light fluctuation. Journal of Experimental Botany, 70, 3705–3708.

Pignon C P, Jaiswal D, Mcgrath J M, Long S P. 2017. Loss of photosynthetic efficiency in the shade. An achilles heel for the dense modern stands of our most productive C4 crops? Journal of Experimental Botany, 68, 335–345.

Sakoda K, Yamori W, Groszmann M, Evans J R. 2021. Stomatal, mesophyll conductance, and biochemical limitations to photosynthesis during induction. Plant Physiology, 185, 146–160.

Soleh M A, Tanaka Y, Kim S Y, Huber S C, Sakoda K, Shiraiwa T. 2017. Identification of large variation in the photosynthetic induction response among 37 soybean [Glycine max (L.) Merr.] genotypes that is not correlated with steady-state photosynthetic capacity. Photosynthesis Research, 131, 305–315.

Soleh M A, Tanaka Y, Nomoto Y, Iwahashi Y, Nakashima K, Fukuda Y, Long S P, Shiraiwa T. 2016. Factors underlying genotypic differences in the induction of photosynthesis in soybean [Glycine max (L.) Merr.]. Plant Cell and Environment, 39, 685–693.

De Souza A P, Burgess S J, Doran L, Hansen J, Manukyan L, Maryn N, Gotarkar D, Leonelli L, Niyogi K K, Long S P. 2022. Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection. Science, 377, 851–854.

De Souza A P, Wang Y, Orr D J, Carmo-Silva E, Long S P. 2020. Photosynthesis across african cassava germplasm is limited by rubisco and mesophyll conductance at steady state, but by stomatal conductance in fluctuating light. New Phytologist, 225, 2498–2512.

Tang C, Luo M, Zhang S, Jia G, Tang S, Jia Y, Zhi H, Diao X. 2023. Variations in chlorophyll content, stomatal conductance, and photosynthesis in setaria ems mutants. Journal of Integrative Agriculture, 22, 1618–1630.

Taylor S H, Long S P. 2017. Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity. Philosophical Transactions of the Royal Society B-Biological Sciences, 372, 20160543.

Théroux-Rancourt G, Earles J M, Gilbert M E, Zwieniecki M A, Boyce C K, Mcelrone A J, Brodersen C R. 2017. The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging. The New Phytologist, 215, 1609–1622.

Tomeo N J, Rosenthal D M. 2017. Variable mesophyll conductance among soybean cultivars sets a tradeoff between photosynthesis and water-use-efficiency. Plant Physiology, 174, 241–257.

Tomimatsu H, Tang Y. 2016. Effects of high CO2 levels on dynamic photosynthesis: carbon gain, mechanisms, and environmental interactions. Journal of Plant Research, 129, 365–377.

Vialet-Chabrand S, Matthews J S, Simkin A J, Raines C A, Lawson T. 2017. Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiology, 173, 2163–2179.

Wang Y, Burgess S J, de Becker E M, Long S P. 2020. Photosynthesis in the fleeting shadows: an overlooked opportunity for increasing crop productivity? Plant Journal, 101, 874–884.

Wang Y, Noguchi K, Ono N, Inoue S, Terashima I, Kinoshita T. 2014. Overexpression of plasma membrane H+-atpase in guard cells promotes light-induced stomatal opening and enhances plant growth. Proceedings of the National Academy of Sciences of the United States of America, 111, 533–538.

Wu H Y, Qiao M Y, Zhang Y J, Kang W J, Ma Q H, Gao H Y, Zhang W F, Jiang C D. 2023. Photosynthetic mechanism of maize yield under fluctuating light environments in the field. Plant Physiology, 191, 957–973.

Wu Y, Wang E, Gong W, Xu L, Zhao Z, Di He, Yang F, Wang X, Yong T, Liu J, Pu T, Yan Y, Yang W. 2023. Soybean yield variations and the potential of intercropping to increase production in china. Field Crops Research, 291, 108771.

Xiong D, Liu X, Liu L, Douthe C, Li Y, Peng S, Huang J. 2015. Rapid responses of mesophyll conductance to changes of CO2 concentration, temperature and irradiance are affected by N supplements in rice. Plant, Cell & Environment, 38, 2541–2550.

Xiong Z, Dun Z, Wang Y, Yang D, Xiong D, Cui K, Peng S, Huang J. 2021. Effect of stomatal morphology on leaf photosynthetic induction under fluctuating light in rice. Frontiers in Plant Science, 12, 754790.

Yamori W, Kusumi K, Iba K, Terashima I. 2020. Increased stomatal conductance induces rapid changes to photosynthetic rate in response to naturally fluctuating light conditions in rice. Plant, Cell & Environment, 43, 1230–1240.

Yao X, Zhou H, Zhu Q, Li C, Zhang H, Wu J J, Xie F. 2017. Photosynthetic response of soybean leaf to wide light-fluctuation in maize–soybean intercropping system. Frontiers in Plant Science, 8, 1695.

Yin X, Struik P C. 2009. Theoretical reconsiderations when estimating the mesophyll conductance to CO2 diffusion in leaves of C3 plants by analysis of combined gas exchange and chlorophyll fluorescence measurements. Plant Cell and Environment, 32, 1513–1524.

Yin X, Sun Z, Struik P C, Gu J. 2011. Evaluating a new method to estimate the rate of leaf respiration in the light by analysis of combined gas exchange and chlorophyll fluorescence measurements. Journal of Experimental Botany, 62, 3489–3499.

Zhang Y, Kaiser E, Marcelis L, Yang Q, Li T. 2020. Salt stress and fluctuating light have separate effects on photosynthetic acclimation, but interactively affect biomass. Plant Cell and Environment, 43, 2192–2206.

Zheng B, Li Y T, Wu Q P, Zhao W, Ren T H, Zhang X H, Li G, Ning T Y, Zhang Z S. 2023. Maize (Zea mays L.) planted at higher density utilizes dynamic light more efficiently. Plant Cell and Environment, 46, 3305–3322.

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