Evaluation of potential increase in photosynthetic efficiency of cassava (Manihot esculenta Crantz) plants exposed to elevated carbon dioxide
V. Ravi A # , Saravanan Raju A and Sanket J. More
A B # *
A
B
Abstract
Cassava (Manihot esculenta Crantz), an important tropical crop, is affected by extreme climatic events, including rising CO2 levels. We evaluated the short-term effect of elevated CO2 concentration (ECO2) (600, 800 and 1000 ppm) on the photosynthetic efficiency of 14 cassava genotypes. ECO2 significantly altered gaseous exchange parameters (net photosynthetic rate (Pn), stomatal conductance (gs), intercellular CO2 (Ci) and transpiration (E)) in cassava leaves. There were significant but varying interactive effects between ECO2 and varieties on these physiological characteristics. ECO2 at 600 and 800 ppm increased the Pn rate in the range of 13–24% in comparison to 400 ppm (ambient CO2), followed by acclimation at the highest concentration of 1000 ppm. A similar trend was observed in gs and E. Conversely, Ci increased significantly and linearly across increasing CO2 concentration. Along with Ci, a steady increase in water use efficiency [WUEintrinsic (Pn/gs) and WUEinstantaneous (Pn/E)] across various CO2 concentrations corresponded with the central role of restricted stomatal activity, a common response under ECO2. Furthermore, Pn had a significant quadratic relationship with the ECO2 (R2 = 0.489) and a significant and linear relationship with Ci (R2 = 0.227). Relative humidity and vapour pressure deficit during the time of measurements remained at 70–85% and ~0.9–1.31 kPa, respectively, at 26 ± 2°C leaf temperature. Notably, not a single variety exhibited constant performance for any of the parameters across CO2 concentrations. Our results indicate that the potential photosynthesis can be increased up to 800 ppm cassava varieties with high sink capacity can be cultivated under protected cultivation to attain higher productivity.
Keywords: cassava, climate change, elevated CO2, food security, Manihot esculenta Crantz, photosynthetic efficiency, stomatal conductance, water use efficiency.
References
AbdElgawad H, Hassan YM, Alotaibi MO, Mohammed AE, Saleh AM (2020) C3 and C4 plant systems respond differently to the concurrent challenges of mercuric oxide nanoparticles and future climate CO2. Science of The Total Environment 749, 142356.
| Crossref | Google Scholar | PubMed |
Ainsworth EA, Long SP (2021) 30 years of free-air carbon dioxide enrichment (FACE): what have we learned about future crop productivity and its potential for adaptation? Global Change Biology 27, 27-49.
| Crossref | Google Scholar | PubMed |
Arora NK (2019) Impact of climate change on agriculture production and its sustainable solutions. Environmental Sustainability 2, 95-96.
| Crossref | Google Scholar |
Avila RT, de Almeida WL, Costa LC, Machado KLG, Barbosa ML, De Souza RPB, Martino PB, Juárez MAT, Marçal DMS, Martins SCV, Ramalho JDC, DaMatta FM (2020) Elevated air [CO2] improves photosynthetic performance and alters biomass accumulation and partitioning in drought-stressed coffee plants. Environmental and Experimental Botany 177, 104137.
| Crossref | Google Scholar |
Becklin KM, Anderson JT, Gerhart LM, Wadgymar SM, Wessinger CA, Ward JK (2016) Examining plant physiological responses to climate change through an evolutionary lens. Plant Physiology 172, 635-649.
| Crossref | Google Scholar |
Becklin KM, Ward JK, Way DA (Eds) (2021) ‘Photosynthesis, respiration, and climate change.’ (Springer International Publishing: Cham, Switzerland) doi:10.1007/978-3-030-64926-5
Bhargava S, Mitra S (2021) Elevated atmospheric CO2 and the future of crop plants. Plant breeding 140, 1-11.
| Crossref | Google Scholar |
Bräutigam A, Gowik U (2016) Photorespiration connects C3 and C4 photosynthesis. Journal of Experimental Botany 67, 2953-2962.
| Crossref | Google Scholar | PubMed |
Bunce J (2021) Carboxylation capacity can limit C3 photosynthesis at elevated CO2 throughout diurnal cycles. Plants 10, 2603.
| Crossref | Google Scholar | PubMed |
Ceballos H, Hershey C, Iglesias C, Zhang X (2021) Fifty years of a public cassava breeding program: evolution of breeding objectives, methods, and decision-making processes. Theoretical and Applied Genetics 134, 2335-2353.
| Crossref | Google Scholar | PubMed |
Cen Y-P, Sage RF (2005) The regulation of rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiology 139, 979-990.
| Crossref | Google Scholar | PubMed |
Chaudhry S, Sidhu GPS (2022) Climate change regulated abiotic stress mechanisms in plants: a comprehensive review. Plant Cell Reports 41, 1-31.
| Crossref | Google Scholar | PubMed |
Chen C-T, Setter TL (2021) Role of tuber developmental processes in response of potato to high temperature and elevated CO2. Plants 10, 871.
| Crossref | Google Scholar | PubMed |
Cock JH, Franklin D, Sandoval G, Juri P (1979) The ideal cassava plant for maximum yield. Crop Science 19, 271-279.
| Crossref | Google Scholar |
Crous KY (2019) Plant responses to climate warming: physiological adjustments and implications for plant functioning in a future, warmer world. American Journal of Botany 106, 1049-1051.
| Crossref | Google Scholar | PubMed |
Cruz JL, Alves AAC, LeCain DR, Ellis DD, Morgan JA (2014) Effect of elevated CO2 concentration and nitrate: ammonium ratios on gas exchange and growth of cassava (Manihot esculenta Crantz). Plant and Soil 374, 33-43.
| Crossref | Google Scholar |
Cruz JL, Alves AAC, LeCain DR, Ellis DD, Morgan JA (2016) Elevated CO2 concentrations alleviate the inhibitory effect of drought on physiology and growth of cassava plants. Scientia Horticulturae 210, 122-129.
| Crossref | Google Scholar |
Cruz JL, LeCain DR, Alves AAC, Coelho Filho MA, Coelho EF (2018) Elevated CO2 reduces whole transpiration and substantially improves root production of cassava grown under water deficit. Archives of Agronomy and Soil Science 64, 1623-1634.
| Crossref | Google Scholar |
Deng Q, Zhou G, Liu J, Liu S, Duan H, Zhang D (2010) Responses of soil respiration to elevated carbon dioxide and nitrogen addition in young subtropical forest ecosystems in China. Biogeosciences 7, 315-328.
| Crossref | Google Scholar |
Dethvongsa S, Vu NA, Van TK (2021) Comparison waterlogging tolerance potential of cassava. IOP Conference Series: Earth and Environmental Science 707, 012002.
| Crossref | Google Scholar |
Dong J, Gruda N, Lam SK, Li X, Duan Z (2018) Effects of elevated CO2 on nutritional quality of vegetables: a review. Frontiers in Plant Science 9, 924.
| Crossref | Google Scholar | PubMed |
El-Sharkawy MA (2016) Prospects of photosynthetic research for increasing agricultural productivity, with emphasis on the tropical C4Amaranthus and the cassava C3-C4 crops. Photosynthetica 54, 161-184.
| Crossref | Google Scholar |
Engineer CB, Ghassemian M, Anderson JC, Peck SC, Hu H, Schroeder JI (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO2 control of stomatal development. Nature 513, 246-250.
| Crossref | Google Scholar | PubMed |
Fernández MD, Tezara W, Rengifo E, Herrera A (2002) Lack of downregulation of photosynthesis in a tropical root crop, cassava, grown under an elevated CO2 concentration. Functional Plant Biology 29, 805.
| Crossref | Google Scholar | PubMed |
Fischer JM, Ward JK (2021) Trichome responses to elevated atmospheric CO2 of the future. In ‘Photosynthesis, respiration, and climate change. Advances in photosynthesis and respiration’. (Eds KM Becklin, JK Ward, DA Way) pp. 103–129. (Springer International Publishing: Cham, Switzerland) doi:10.1007/978-3-030-64926-5_5
Forbes SJ, Cernusak LA, Northfield TD, Gleadow RM, Lambert S, Cheesman AW (2020) Elevated temperature and carbon dioxide alter resource allocation to growth, storage and defence in cassava (Manihot esculenta). Environmental and Experimental Botany 173, 103997.
| Crossref | Google Scholar |
Gleadow RM, Evans JR, McCaffery S, Cavagnaro TR (2009) Growth and nutritive value of cassava (Manihot esculenta Cranz.) are reduced when grown in elevated CO2. Plant Biology 11, 76-82.
| Crossref | Google Scholar | PubMed |
Gojon A, Cassan O, Bach L, Lejay L, Martin A (2022) The decline of plant mineral nutrition under rising CO2: physiological and molecular aspects of a bad deal. Trends in Plant Science
| Crossref | Google Scholar |
Habib-ur-Rahman M, Ahmad A, Raza A, Hasnain MU, Alharby HF, Alzahrani YM, Bamagoos AA, Hakeem KR, Ahmad S, Nasim W, Ali S, Mansour F, El Sabagh A (2022) Impact of climate change on agricultural production; issues, challenges, and opportunities in Asia. Frontiers in Plant Science 13, 925548.
| Crossref | Google Scholar |
Hogan KP, Smith AP, Ziska LH (1991) Potential effects of elevated CO2 and changes in temperature on tropical plants. Plant, Cell and Environment 14, 763-778.
| Crossref | Google Scholar |
Imai K, Coleman DF, Yanagisawa T (1984) Elevated atmospheric partial pressure of carbon dioxide and dry matter production of cassava. Japanese Journal of Crop Science 53, 479-485.
| Crossref | Google Scholar |
IPCC (2021) Summary for Policymakers. In ‘Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds V Masson-Delmotte, P Zhai, A Pirani, SL Connors, C Péan, S Berger, N Caud, Y Chen, L Goldfarb, MI Gomis, M Huang, K Leitzell, E Lonnoy, JBR Matthews, TK Maycock, T Waterfield, O Yelekçi, R Yu, B Zhou) pp. 3–32. (Cambridge University Press: Cambridge, UK). doi:10.1017/9781009157896.001
Jansson C, Westerbergh A, Zhang J, Hu X, Sun C (2009) Cassava, a potential biofuel crop in (the) People’s Republic of China. Applied Energy 86, S95-S99.
| Crossref | Google Scholar |
Kadam NN, Xiao G, Melgar RJ, Bahuguna RN, Quinones C, Tamilselvan A, Prasad PVV, Jagadish KSV (2014) Agronomic and physiological responses to high temperature, drought, and elevated CO2 interactions in cereals. In ‘Advances in Agronomy’. (Ed. D Sparks) pp. 111–156. (Elsevier) doi:10.1016/B978-0-12-800131-8.00003-0
Kang H, Zhu T, Zhang Y, Ke X, Sun W, Hu Z, Zhu X, Shen H, Huang Y, Tang Y (2021) Elevated CO2 enhances dynamic photosynthesis in rice and wheat. Frontiers in Plant Science 12, 727374.
| Crossref | Google Scholar | PubMed |
Katul G, Manzoni S, Palmroth S, Oren R (2010) A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration. Annals of Botany 105, 431-442.
| Crossref | Google Scholar | PubMed |
Keenan TF, Hollinger DY, Bohrer G, Dragoni D, Munger JW, Schmid HP, Richardson AD (2013) Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. Nature 499, 324-327.
| Crossref | Google Scholar | PubMed |
Kumari A, Lakshmi GA, Krishna GK, Patni B, Prakash S, Bhattacharyya M, Singh SK, Verma KK (2022) Climate change and its impact on crops: a comprehensive investigation for sustainable agriculture. Agronomy 12, 3008.
| Crossref | Google Scholar |
Lal MK, Sharma N, Adavi SB, Sharma E, Altaf MA, Tiwari RK, Kumar R, Kumar A, Dey A, Paul V, Singh B, Singh MP (2022) From source to sink: mechanistic insight of photoassimilates synthesis and partitioning under high temperature and elevated [CO2]. Plant Molecular Biology 110, 305-324.
| Crossref | Google Scholar | PubMed |
Lawson T, Craigon J, Black CR, Colls JJ, Tulloch A-M, Landon G (2001) Effects of elevated carbon dioxide and ozone on the growth and yield of potatoes (Solanum tuberosum) grown in open-top chambers. Environmental Pollution 111, 479-491.
| Crossref | Google Scholar | PubMed |
Li S, Li X, Wei Z, Liu F (2020) ABA-mediated modulation of elevated CO2 on stomatal response to drought. Current Opinion in Plant Biology 56, 174-180.
| Crossref | Google Scholar | PubMed |
Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant, Cell & Environment 14, 729-739.
| Crossref | Google Scholar |
Malik AI, Kongsil P, Nguyễn VA, Ou W, Sholihin, Srean P, Sheela M, Becerra López-Lavalle LA, Utsumi Y, Lu C, Kittipadakul P, Nguyễn HH, Ceballos H, Nguyễn TH, Selvaraj Gomez M, Aiemnaka P, Labarta R, Chen S, Amawan S, Sok S, Youabee L, Seki M, Tokunaga H, Wang W, Li K, Nguyễn HA, Nguyễn VĐ, Hàm LH, Ishitani M (2020) Cassava breeding and agronomy in Asia: 50 years of history and future directions. Breeding Science 70, 145-166.
| Crossref | Google Scholar | PubMed |
More SJ, Ravi V, Suresh Kumar J (2019a) Cassava under water deficit stress: differential carbon isotope discrimination. In ‘National Conference of Plant Physiology NCPP-2019 Plant Productivity and Stress Management’. Department of Plant Physiology, Kerala Agricultural University, Thrissur, Kerala, 19–21 December 2019. (Kerala Agricultural University: India)
More SJ, Ravi V, Raju S (2019b) Tropical tuber crops. In ‘Postharvest physiological disorders in fruits and vegetables’. (Eds S Tonetto de Freitas, S Pareek) pp. 719–758. (CRC Press: Boca Raton, FL, USA) doi:10.1201/b22001
More SJ, Ravi V, Raju S, Suresh Kumar J (2020) The quest for high yielding drought-tolerant cassava variety. Journal of Pharmacognosy and Phytochemistry 9(6S), 433-439.
| Google Scholar |
More SJ, Bardhan K, Ravi V, Pasala R, Chaturvedi AK, Lal MK, Siddique KHM (2023) Morphophysiological responses and tolerance mechanisms in cassava (Manihot esculenta Crantz) under drought stress. Journal of Soil Science and Plant Nutrition 21, 71-91.
| Crossref | Google Scholar |
Nadal M, Carriquí M, Flexas J (2021) Mesophyll conductance to CO2 diffusion in a climate change scenario: effects of elevated CO2, temperature and water stress. In ‘Photosynthesis, respiration, and climate change’. Advances in photosynthesis and respiration. (Eds KM Becklin, JK Ward, DA Way) pp. 49–78. (Springer International Publishing: Cham, Switzerland) doi:10.1007/978-3-030-64926-5_3
NASA (2023) Climate Change Evidence: How Do We Know? Climate Change: Vital Signs of the Planet. Available at https://climate.nasa.gov/evidence [accessed 1 April 2023]
Negi J, Hashimoto-Sugimoto M, Kusumi K, Iba K (2014) New approaches to the biology of stomatal guard cells. Plant and Cell Physiology 55, 241-250.
| Crossref | Google Scholar | PubMed |
NOAA (2023) Climate Change: Atmospheric Carbon Dioxide. NOAA Climate. Available at http://www.climate.gov/news-features/understanding-climate/climate-change-atmospheric-carbon-dioxide [accessed 1 April 2023]
Okogbenin E, Setter TL, Ferguson M, Mutegi R, Ceballos H, Olasanmi B, Fregene M (2013) Phenotypic approaches to drought in cassava: review. Frontiers in Physiology 4, 93.
| Crossref | Google Scholar |
Pan C, Ahammed GJ, Li X, Shi K (2018) Elevated CO2 improves photosynthesis under high temperature by attenuating the functional limitations to energy fluxes, electron transport and redox homeostasis in tomato leaves. Frontiers in Plant Science 9, 1739.
| Crossref | Google Scholar | PubMed |
Poorter H, Knopf O, Wright IJ, Temme AA, Hogewoning SW, Graf A, Cernusak LA, Pons TL (2022) A meta-analysis of responses of C3 plants to atmospheric CO2: dose–response curves for 85 traits ranging from the molecular to the whole-plant level. New Phytologist 233, 1560-1596.
| Crossref | Google Scholar | PubMed |
Ravi V, Saravanan R, Byju G, Nair KP, James G (2017) Photosynthetic response of sweet potato (Ipomoea batatas) to photon flux density and elevated carbon dioxide. The Indian Journal of Agricultural Sciences 87(9), 1231-1237.
| Crossref | Google Scholar |
Ravi V, More SJ, Saravanan R, Pallavi Nair K, Byju G (2018) Evaluation of photosynthetic efficiency of elephant-foot yam (Amorphophallus paeoniifolius) to photon flux density and elevated CO2. Current Horticulture 6(1), 55-63.
| Google Scholar |
Ravi V, More SJ, Saravanan R, Byju G, Nedunchezhiyan M, Aasha Devi A, Pallavi Nair K (2019) Potential increase in photosynthetic response of taro (Colocasia esculenta L.) to photon flux density and elevated CO2. Journal of Environmental Biology 40, 111-118.
| Crossref | Google Scholar |
Ravi V, Pushpaleela A, Raju S, Gangadharan B, More SJ (2020) Evaluation of photosynthetic efficiency of yam bean (Pachyrhizus erosus L.) at saturating photon flux density under elevated carbon dioxide. Physiology and Molecular Biology of Plants 26, 189-194.
| Crossref | Google Scholar | PubMed |
Ravi V, Suja G, Saravanan R, More SJ (2021) Advances in cassava-based multiple-cropping systems. In ‘Horticultural reviews’. (Ed. I Warrington) pp. 153–232. (Wiley) doi:10.1002/9781119750802.ch3
Ravi V, More SJ, Raju S, Muthuraj R, Suja G (2022) Assessment of photosynthetic efficiency of greater yam and white yam subjected to elevated carbon dioxide. South African Journal of Botany 145, 397-404.
| Crossref | Google Scholar |
Razzaque M, Haque MM, Hamid A (2010) Elevated CO2 and nitrogen interaction in photosynthesis and productivity of modern and local rice (Oryza sativa L.) cultivars. The Agriculturists 105-112.
| Crossref | Google Scholar |
Rosenthal DM, Slattery RA, Miller RE, Grennan AK, Cavagnaro TR, Fauquet CM, Gleadow RM, Ort DR (2012) Cassava about-FACE: greater than expected yield stimulation of cassava (Manihot esculenta) by future CO2 levels. Global Change Biology 18, 2661-2675.
| Crossref | Google Scholar |
Ruiz-Vera UM, De Souza AP, Ament MR, Gleadow RM, Ort DR (2021) High sink strength prevents photosynthetic down-regulation in cassava grown at elevated CO2 concentration. Journal of Experimental Botany 72, 542-560.
| Crossref | Google Scholar |
Ruiz-Vera UM, Balikian R, Larson TH, Ort DR (2023) Evaluation of the effects of elevated CO2 concentrations on the growth of cassava storage roots by destructive harvests and ground penetrating radar scanning approaches. Plant, Cell & Environment 46, 93-105.
| Crossref | Google Scholar | PubMed |
Runion GB, Prior SA, Monday TA, Ryan-Bohac J (2018) Effects of elevated CO2 on growth of the industrial sweetpotato cultivar CX-1. Environment Control in Biology 56, 89-92.
| Crossref | Google Scholar |
Saleh AM, Hassan YM, Selim S, AbdElgawad H (2019) NiO-nanoparticles induce reduced phytotoxic hazards in wheat (Triticum aestivum L.) grown under future climate CO2. Chemosphere 220, 1047-1057.
| Crossref | Google Scholar | PubMed |
Saleh AM, Hassan YM, Habeeb TH, Alkhalaf AA, Hozzein WN, Selim S, AbdElgawad H (2021) Interactive effects of mercuric oxide nanoparticles and future climate CO2 on maize plant. Journal of Hazardous Materials 401, 123849.
| Crossref | Google Scholar | PubMed |
Santanoo S, Vongcharoen K, Banterng P, Vorasoot N, Jogloy S, Roytrakul S, Theerakulpisut P (2022) Physiological and proteomic responses of cassava to short-term extreme cool and hot temperature. Plants 11, 2307.
| Crossref | Google Scholar | PubMed |
Shabbaj II, AbdElgawad H, Balkhyour MA, Tammar A, Madany MMY (2022) Elevated CO2 differentially mitigated oxidative stress induced by indium oxide nanoparticles in young and old leaves of C3 and C4 crops. Antioxidants 11, 308.
| Crossref | Google Scholar | PubMed |
Shanker AK, Gunnapaneni D, Bhanu D, Vanaja M, Lakshmi NJ, Yadav SK, Prabhakar M, Singh VK (2022) Elevated CO2 and water stress in combination in plants: brothers in arms or partners in crime? Biology 11, 1330.
| Crossref | Google Scholar | PubMed |
Silva RG da, Alves R de C, Zingaretti SM (2020) Increased [CO2] causes changes in physiological and genetic responses in C4 crops: a brief review. Plants 9, 1567.
| Crossref | Google Scholar |
Song YG, Hwang JE, An J, Kim PB, Park HB, Park HJ, Kim S, Lee CW, Lee BD, Kim NY, Lee KC (2022) The growth and physiological characteristics of the endangered CAM Plant, Nadopungnan (Sedirea japonica), under drought and climate change scenarios. Forests 13, 1823.
| Crossref | Google Scholar |
Stevens J, Faralli M, Wall S, Stamford JD, Lawson T (2021) Stomatal responses to climate change. In ‘Photosynthesis, respiration, and climate change. Advances in photosynthesis and respiration’. (Eds KM Becklin, JK Ward, DA Way) pp. 17–47. (Springer International Publishing: Cham) doi:10.1007/978-3-030-64926-5_2
Thompson M, Gamage D, Hirotsu N, Martin A, Seneweera S (2017) Effects of elevated carbon dioxide on photosynthesis and carbon partitioning: a perspective on root sugar sensing and hormonal crosstalk. Frontiers in Physiology 8, 578.
| Crossref | Google Scholar | PubMed |
Voss I, Sunil B, Scheibe R, Raghavendra AS (2013) Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biology 15, 713-722.
| Crossref | Google Scholar |
Wang X, Liu F (2021) Effects of elevated CO2 and heat on wheat grain quality. Plants 10, 1027.
| Crossref | Google Scholar | PubMed |
Wang F, Gao J, Yong JWH, Wang Q, Ma J, He X (2020) Higher atmospheric CO2 levels favor C3 plants over C4 plants in utilizing ammonium as a nitrogen source. Frontiers in Plant Science 11, 537443.
| Crossref | Google Scholar | PubMed |
Wei Z, Abdelhakim LOA, Fang L, Peng X, Liu J, Liu F (2022) Elevated CO2 effect on the response of stomatal control and water use efficiency in amaranth and maize plants to progressive drought stress. Agricultural Water Management 266, 107609.
| Crossref | Google Scholar |
Xiao L, Liu GB, Xue S (2016) Elevated CO2 concentration and drought stress exert opposite effects on plant biomass, nitrogen, and phosphorus allocation in Bothriochloa ischaemum. Journal of Plant Growth Regulation 35, 1088-1097.
| Crossref | Google Scholar |
Xu Z, Shimizu H, Yagasaki Y, Ito S, Zheng Y, Zhou G (2013) Interactive effects of elevated CO2, drought, and warming on plants. Journal of Plant Growth Regulation 32, 692-707.
| Crossref | Google Scholar |
Xu Z, Jiang Y, Jia B, Zhou G (2016) Elevated-CO2 response of stomata and its dependence on environmental factors. Frontiers in Plant Science 7, 657.
| Crossref | Google Scholar |
Yamamoto Y, Negi J, Wang C, Isogai Y, Schroeder JI, Iba K (2016) The transmembrane region of guard cell SLAC1 channels perceives CO2 signals via an ABA-independent pathway in Arabidopsis. The Plant Cell 28, 557-567.
| Crossref | Google Scholar | PubMed |
Zheng Y, Li F, Hao L, Yu J, Guo L, Zhou H, Ma C, Zhang X, Xu M (2019) Elevated CO2 concentration induces photosynthetic down-regulation with changes in leaf structure, non-structural carbohydrates and nitrogen content of soybean. BMC Plant Biology 19, 255.
| Crossref | Google Scholar | PubMed |
