Abstract
Low phosphorus (P) availability is a major problem for cotton production. However, little is known about cotton agronomic and physiological traits associated with low P tolerance. Therefore, the agronomic and physiological performance of three cotton genotypes with strong tolerance to low P (STGs) and three cotton genotypes with weak tolerance (WTGs) was characterized under low and normal P conditions in hydroponic and pot culture. The results showed that low P significantly reduced dry matter production, photosynthesis, and carbon metabolism in both STGs and WTGs; however, the reduction was more in WTGs. In contrast, low P improved root morphology, carbohydrate accumulation, and P metabolism, especially in STGs genotype Jimian169, whereas the opposite responses were observed for WTGs mainly DES926. The multivariate analysis suggested that root morphological traits, carbohydrate contents, and enzymes related to P metabolism were strong positively correlated and contributed more to the genotypic variation, suggesting the importance of root over shoot in low P tolerance. Moreover, plants grown under low P produced low yields than normal P, whereas WTGs yields were lower than the STGs yield. Overall, it was suggested that the low P tolerance of cotton genotypes is closely related to root morphology and physiology. In the future, the identified contrasting low P tolerant cotton genotypes Jimian169 and DES926 will be used to understand the molecular mechanisms of low P tolerance in cotton.
Similar content being viewed by others
References
Abbas M, Shah JA, Irfan M, Memon MYJJoPN (2018) Remobilization and utilization of phosphorus in wheat cultivars under induced phosphorus deficiency. J Plant Nutr 41(12):1522–1533
Abenavoli MR, Longo C, Lupini A, Miller AJ, Araniti F, Mercati F, Princi MP, Sunseri FJPP, Biochemistry (2016) Phenotyping two tomato genotypes with different nitrogen use efficiency. Plant Physiol Biochem 107:21–32
Ahmad I, Zhou G, Zhu G, Ahmad Z, Song X, Hao G, Jamal Y, Ibrahim MEHJPJB (2021) Response of leaf characteristics of BT cotton plants to ratio of nitrogen, phosphorus, and potassium. Pak J Bot 53(3):873–881
Akhtar M, Oki Y, Adachi T (2008) Genetic variability in phosphorus acquisition and utilization efficiency from sparingly soluble P-sources by Brassica cultivars under P-stress environment. J Agron Crop Sci 194(5):380–392
Alam S (2003) Wheat yield and P fertilizer efficiency as influenced by rate andintegrated use of chemical and organic fertilizers. Pak J Soil Sci 22(2):72–76
Asif I, Dong Q, Wang X, Gui H, Zhang H, Pang N, Zhang X, Song M (2021) Genotypic variation in root morphology, cotton subtending leaf physiology and fiber quality against nitrogen. J Cotton Res 4(1):1–14
Aslam M, Memon M, Khan P, Imtiaz MJS, Environment (2009) Performance of fertigation technique for phosphorus application in cotton. Soil Environ 28(1):45–48
Aziz T, Lambers H, Nicol D, Ryan MH (2015) Mechanisms for tolerance of very high tissue phosphorus concentrations in P tilotus polystachyus. Plant Cell Environ 38(4):790–799
Baker A, Ceasar SA, Palmer AJ, Paterson JB, Qi W, Muench SP, Baldwin SAJJoeb (2015) Replace, reuse, recycle: improving the sustainable use of phosphorus by plants. J Exp Bot 66(12):3523–3540
Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach. Wiley 90–113:1995
Bayuelo-Jiménez JS, Gallardo-Valdéz M, Pérez-Decelis VA, Magdaleno-Armas L, Ochoa I, Lynch JPJFCR (2011) Genotypic variation for root traits of maize (Zea mays L.) from the Purhepecha Plateau under contrasting phosphorus availability. Field Crops Res 121(3):350–362
Brooks AJFPB (1986) Effects of phosphorus nutrition on ribulose-1, 5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves. Funct Plant Biol 13(2):221–237
Buckley C, Wall DP, Moran B, Murphy PN (2015) Developing the EU Farm Accountancy Data Network to derive indicators around the sustainable use of nitrogen and phosphorus at farm level. Nutr Cycl Agroecosyst 102(3):319–333
Cai J, Chen L, Qu H, Lian J, Liu W, Hu Y, Xu GJAPP (2012) Alteration of nutrient allocation and transporter genes expression in rice under N, P, K, and Mg deficiencies. Acta Physiol Plant 34(3):939–946
Cakmak I, Hengeler C, Marschner HJJoEB (1994) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. J Exp Bot 45(9):1251–1257
Carstensen A, Herdean A, Schmidt SB, Sharma A, Spetea C, Pribil M, Husted SJPp (2018) The impacts of phosphorus deficiency on the photosynthetic electron transport chain. Plant Physiol 177(1):271–284
Chen S, Hajirezaei M, Peisker M, Tschiersch H, Sonnewald U, Börnke FJP (2005) Decreased sucrose-6-phosphate phosphatase level in transgenic tobacco inhibits photosynthesis, alters carbohydrate partitioning, and reduces growth. Planta 221(4):479–492
Cheptoek RP, Gitari HI, Mochoge B, Kisaka OM, Otieno E, Maitra S, Nasar J, Seleiman MFJIJBS (2021) Maize productivity, economic returns and phosphorus use efficiency as influenced by lime, Minjingu rock phosphate and NPK inorganic fertilizer. Int J Bioresour Sci 8:47–60
Ciereszko I, Zambrzycka A, Rychter AJPS (1998) Sucrose hydrolysis in bean roots (Phaseolus vulgaris L.) under phosphate deficiency. Plant Sci 133(2):139–144
Clemens S, Hell R, Mendal R (2010) Cell biology of metals and nutrients, plant cell monographs
Cock J, Yoshida S, Forno DA (1976) Laboratory manual for physiological studies of rice. Int Rice Res Inst 1:1
Crafts-Brandner SJ (1992) Phosphorus nutrition influence on leaf senescence in soybean. Plant Physiol 98(3):1128–1132
De Groot CC, Marcelis LF, van den Boogaard R, Kaiser WM, Lambers HJP, Soil (2003) Interaction of nitrogen and phosphorus nutrition in determining growth. Plant Soil 248(1):257–268
Dissanayaka D, Plaxton WC, Lambers H, Siebers M, Marambe B, Wasaki JJP, Cell E (2018) Molecular mechanisms underpinning phosphorus-use efficiency in rice. Plant Cell Environ 41(7):1483–1496
Dordas CJEJoa (2009) Dry matter, nitrogen and phosphorus accumulation, partitioning and remobilization as affected by N and P fertilization and source–sink relations. Eur J Agron 30(2):129–139
Echer FR, Cordeiro CFdS, de la Torre EdJRJJoPN (2020) The effects of nitrogen, phosphorus, and potassium levels on the yield and fiber quality of cotton cultivars. J Plant Nutr 43(7):921–932
El Mazlouzi M, Morel C, Chesseron C, Robert T, Mollier AJFips (2020a) Contribution of external and internal phosphorus sources to grain P loading in durum wheat (Triticum durum L.) grown under contrasting P levels. Front Plant Sci 870:1
El Mazlouzi M, Morel C, Robert T, Yan B, Mollier AJP, Soil (2020b) Phosphorus uptake and partitioning in two durum wheat cultivars with contrasting biomass allocation as affected by different P supply during grain filling. Plant Soil 449(1):179–192
Elliott GC, Läuchli AJAJ (1985) Phosphorus efficiency and phosphate-iron interaction in maize 1. Agron J 77(3):399–403
Galle A, Florez-Sarasa I, Tomas M, Pou A, Medrano H, Ribas-Carbo M, Flexas JJJoEB (2009) The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? J Exp Bot 60(8):2379–2390
Gan Y, Stulen I, Van Keulen H, Kuiper PJ (2002) Physiological changes in soybean (Glycine max) Wuyin9 in response to N and P nutrition. Ann Appl Biol 140(3):319–329
García-Caparrós P, Lao MT, Preciado-Rangel P, Sanchez EJA (2021) Phosphorus and carbohydrate metabolism in green bean plants subjected to increasing phosphorus concentration in the nutrient solution. Agronomy 11(2):245
Ghaffar S, Stevenson RJ, Khan Z (2017) Effect of phosphorus stress on Microcystis aeruginosa growth and phosphorus uptake. PLoS ONE 12(3):e0174349
Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59(1):93–109
He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang ZJPP (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus× canescens. Physiol Plant 143(1):50–63
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198
Hermans C, Hammond JP, White PJ, Verbruggen NJTips (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11(12):610–617
Iqbal A, Dong Q, Wang X, Gui H, Zhang H, Zhang X, Song M (2020a) High nitrogen enhance drought tolerance in cotton through antioxidant enzymatic activities, nitrogen metabolism and osmotic adjustment. Plants 9(2):178
Iqbal A, Dong Q, Wang X, Gui H, Zhang H, Zhang X, Song M (2020b) Variations in nitrogen metabolism are closely linked with nitrogen uptake and utilization efficiency in cotton genotypes under various nitrogen supplies. Plants 9(2):250
Iqbal A, Dong Q, Wang X, Gui HP, Zhang H, Pang N, Zhang X, Song M (2020c) Nitrogen preference and genetic variation of cotton genotypes for nitrogen use efficiency. J Sci Food Agric 100(6):2761–2773
Iqbal A, Gui H, Zhang H, Wang X, Pang N, Dong Q, Song M (2019a) Genotypic variation in cotton genotypes for phosphorus-use efficiency. Agronomy 9(11):689
Iqbal A, Jing N, Qiang D, Xiangru W, Huiping G, Hengheng Z, Nianchang P, Xiling Z, Meizhen S (2022a) Physiological characteristics of cotton subtending leaf are associated with yield in contrasting nitrogen-efficient cotton genotypes. Front Plant Sci 13:825116–825116
Iqbal A, Qiang D, Xiangru W, Huiping G, Jing N, Leilei L, Hengheng Z, Nianchang P, Xiling Z, Meizhen S (2022b) N-efficient cotton genotype grown under low nitrogen shows relatively large root system, high biomass accumulation and nitrogen metabolism. Agron J 114(1):582–600
Iqbal A, Qiang D, Zhun W, Xiangru W, Huiping G, Hengheng Z, Nianchang P, Xiling Z, Meizhen S (2020d) Growth and nitrogen metabolism are associated with nitrogen-use efficiency in cotton genotypes. Plant Physiol Biochem 149:61–74
Iqbal A, Song M, Shah Z, Alamzeb M, Iqbal M (2019b) Integrated use of plant residues, phosphorus and beneficial microbes improve hybrid maize productivity in semiarid climates. Acta Ecol Sin 39(5):348–355
Jacob J, Lawlor D (1993) Extreme phosphate deficiency decreases the in vivo CO2/O2 specificity factor of ribulose 1, 5-bisphosphate carboxylase-oxygenase in intact leaves of sunflower. J Exp Bot 44(11):1635–1641
Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KGJP (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225(4):907–918
Katkar R, Turkhade A, Solanke U (2002) Effect of foliar sprays of nutrients and chemicals on yield and quality of cotton under rainfed condition. Res Crops 3(1):27–29
Kim H-J, Li X (2016) Effects of phosphorus on shoot and root growth, partitioning, and phosphorus utilization efficiency in Lantana. HortScience 51(8):1001–1009
Kosar H, Gill M, Aziz T, Tahir M (2003) Relative phosphorus utilization efficiency of wheat genotypes in hydroponics. Pak J Agric Sci 40(1–2):28–32
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98(4):693–713
Lawlor DJJEB (2002) Ecophysiology and agronomy: carbon and nitrate 53:773–787
Li H, Liu J, Li G, Shen J, Bergström L, Zhang F (2015) Past, present, and future use of phosphorus in Chinese agriculture and its influence on phosphorus losses. Ambio 44(2):274–285
Liang C, Tian J, Lam H-M, Lim BL, Yan X, Liao HJPp (2010) Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiol 152(2):854–865
Ling Q, Yang JJSAS (1986) Studies on “grain-leaf ratio” of population and cultural approaches of high yield in rice plants. Sci Agric Sin 19(3):1–8
Liu J, Peng J, Xia H, Li P, Li Z, Sun M, Zheng C, Dong HJJoPGR (2021) High soil available phosphorus favors carbon metabolism in cotton leaves in pot trials. J Plant Growth Regul 40(3):974–985
Liu J, Wang Y, Chen J, Lv F, Ma Y, Meng Y, Chen B, Zhou ZJTJoAS (2014) Sucrose metabolism in the subtending leaf to cotton boll at different fruiting branch nodes and the relationship to boll weight. J Agric Sci 152(5):790–804
Liu Z, Gao K, Shan S, Gu R, Wang Z, Craft EJ, Mi G, Yuan L, Chen F (2017) Comparative analysis of root traits and the associated QTLs for maize seedlings grown in paper roll, hydroponics and vermiculite culture system. Front Plant Sci 8:436
Loewe A, Einig W, Shi L, Dizengremel P, Hampp RJTNP (2000) Mycorrhiza formation and elevated CO2 both increase the capacity for sucrose synthesis in source leaves of spruce and aspen. New Phytol 145(3):565–574
López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella LJAropb (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123
Lynch J, Brown K (2006) Whole plant adaptations to low phosphorus availability. In: Huang B (ed) Plant–environment interactions’, 3rd edn. Taylor and Francis, New York
Ma Q, Rengel Z, Siddique KH (2011) Wheat and white lupin differ in root proliferation and phosphorus use efficiency under heterogeneous soil P supply. Crop Pasture Sci 62(6):467–473
Masoni A, Ercoli L, Mariotti M, Arduini IJEJoA (2007) Post-anthesis accumulation and remobilization of dry matter, nitrogen and phosphorus in durum wheat as affected by soil type. Eur J Agron 26(3):179–186
Nadira UA, Ahmed IM, Zeng J, Bibi N, Cai S, Wu F, Zhang G (2014) The changes in physiological and biochemical traits of Tibetan wild and cultivated barley in response to low phosphorus stress. Soil Sci Plant Nutr 60(6):832–842
Niu J, Gui H, Iqbal A, Zhang H, Dong Q, Pang N, Wang S, Wang Z, Wang X, Yang G (2020) N-use efficiency and yield of cotton (G. hirsutism L.) are improved through the combination of N-fertilizer reduction and N-efficient cultivar. Agronomy 11(1):55
Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112(2):391–408
Pang J, Zhao H, Bansal R, Bohuon E, Lambers H, Ryan MH, Siddique KH (2018) Leaf transpiration plays a role in phosphorus acquisition among a large set of chickpea genotypes. Plant Cell Environ 41(9):2069–2079
Paul M, Stitt MJP, Cell E (1993) Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose. Plant Cell Environ 16(9):1047–1057
Plaxton W, Lambers H (2015) Annual plant reviews, phosphorus metabolism in plants, vol 48. Wiley
Rao IM, Fredeen AL, Terry NJPP (1990) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet: III Diurnal changes in carbon partitioning and carbon export. Plant Physiol 92(1):29–36
Rose TJ, Rose MT, Pariasca-Tanaka J, Heuer S, Wissuwa M (2011) The frustration with utilization: why have improvements in internal phosphorus utilization efficiency in crops remained so elusive? Front Plant Sci 2:73
Saleem M, Cheema M, Bilal M, Anjum S, Shahid M, Khurshid IJTJoA, Sciences P (2011) Fiber quality of cotton (Gossypium hirsutum) cultivars under different phosphorus levels. J Anim Plant Sci 21:26–30
Samejima H, Kondo M, Ito O, Nozoe T, Shinano T, Osaki MJJopn (2005) Characterization of root systems with respect to morphological traits and nitrogen-absorbing ability in the new plant type of tropical rice lines. J Plant Nutr 28(5):835–850
Samejima H, Kondo M, Ito O, Nozoe T, Shinano T, Osaki MJSS, Nutrition P (2004) Root-shoot interaction as a limiting factor of biomass productivity in new tropical rice lines. Soil Sci Plant Nutr 50(4):545–554
Sarkar R, Majumdar RJIjoas (2002) Effect of farmyard manure, nitrogen and phosphorus on yield and fibre quality of upland cotton (Gossypium hirsutum) in rice fallow land. Biores Technol 72(10):607–610
Sawan ZM, Mahmoud MH, El-Guibali AHJJoPE (2008) Influence of potassium fertilization and foliar application of zinc and phosphorus on growth, yield components, yield and fiber properties of Egyptian cotton (Gossypium barbadense L.). J Plant Ecol 1(4):259–270
Seleiman MF (2019) Use of plant nutrients in improving abiotic stress tolerance in wheat. Wheat Production in Changing Environments. Springer, Beijing, pp 481–495
Seleiman MF, Abdelaal MSJEJoA (2018) Effect of organic, inorganic and bio-fertilization on growth, yield and quality traits of some chickpea (Cicer arietinum L.) varieties. Egypt J Agron 40(1):105–117
Seleiman MF, Almutairi KF, Alotaibi M, Shami A, Alhammad BA, Battaglia MLJP (2020a) Nano-fertilization as an emerging fertilization technique: why can modern agriculture benefit from its use? Plants 10(1):2
Seleiman MF, Santanen A, Mäkelä PSJR, Conservation R (2020b) Recycling sludge on cropland as fertilizer–advantages and risks. Resour Conserv Recycl 155:104647
Siddiqi MY, Glass ADJJopn, (1981) Utilization index: a modified approach to the estimation and comparison of nutrient utilization efficiency in plants. J Plant Nutr 4(3):289–302
Snapp SS, Lynch JP (1996) Phosphorus distribution and remobilization in bean plants as influenced by phosphorus nutrition. Crop Sci 36(4):929–935
Srinivasarao C, Ganeshamurthy A, Ali M, Venkateswarlu B (2006) Phosphorus and micronutrient nutrition of chickpea genotypes in a multi-nutrient-deficient typic ustochrept. J Plant Nutr 29(4):747–763
Taliman NA, Dong Q, Echigo K, Raboy V, Saneoka HJP (2019) Effect of phosphorus fertilization on the growth, photosynthesis, nitrogen fixation, mineral accumulation, seed yield, and seed quality of a soybean low-phytate line. Plants 8(5):119
Tariq Aziz P, Maqsood MA, Mansoor T (2005) Differences in phosphorus absorption, transport and utilization by twenty rice (Oryza sativa L.) cultivars. Pak J Agri Sci 42:3–4
Thuynsma R, Kleinert A, Kossmann J, Valentine AJ, Hills PN (2016) The effects of limiting phosphate on photosynthesis and growth of Lotus japonicus. S Afr J Bot 104:244–248
Usuda H, Shimogawara KJP, physiology c, (1991) Phosphate deficiency in maize. II. Enzyme activities. Plant Cell Physiol 32(8):1313–1317
Vance CP, Uhde-Stone C (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157(3):423–447
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195(2):306–320
Veronica N, Subrahmanyam D, Vishnu Kiran T, Yugandhar P, Bhadana V, Padma V, Jayasree G, Voleti SJP (2017) Influence of low phosphorus concentration on leaf photosynthetic characteristics and antioxidant response of rice genotypes. Photosynthetica 55(2):285–293
Villar-Salvador P, Peñuelas JL, Jacobs DF (2013) Nitrogen nutrition and drought hardening exert opposite effects on the stress tolerance of Pinus pinea L. seedlings. Tree Physiol 33(2):221–232
Wang H, Inukai Y (2006) Root development and nutrient uptake. Crit Rev Plant Sci 25(3):279–301
Wang Z, Li D, Li G, Liu YJHA (2010) Mechanism of photosynthetic response in Microcystis aeruginosa PCC7806 to low inorganic phosphorus. Harmful Algae 9(6):613–619
Wasaki J, Shinano T, Onishi K, Yonetani R, Yazaki J, Fujii F, Shimbo K, Ishikawa M, Shimatani Z, Nagata YJJoeb (2006) Transcriptomic analysis indicates putative metabolic changes caused by manipulation of phosphorus availability in rice leaves. J Exp Bot 57(9):2049–2059
Wissuwa M, Ae NJP (2001) Further characterization of two QTLs that increase phosphorus uptake of rice (Oryza sativa L.) under phosphorus deficiency. Plant Soil 237(2):275–286
Wissuwa MJPp (2003) How do plants achieve tolerance to phosphorus deficiency? Small causes with big effects. Plant Physiol 133(4):1947–1958
Xu X, Yang Y, Liu C, Sun Y, Zhang T, Hou M, Huang S, Yuan HJBpb (2019) The evolutionary history of the sucrose synthase gene family in higher plants. BMC Plant Biol 19(1):1–14
Yang C, Liu R, Zhang G, Xu L, Zhou ZJAAS (2014) Effects of waterlogging on sucrose metabolism of the subtending leaf of cotton boll and boll weight during flowering and boll-forming stage. Plant Sci 40(5):908–914
Yang J-c, Zhang H, J-hJJoIA Z (2012) Root morphology and physiology in relation to the yield formation of rice. J Integr Agric 11(6):920–926
Yang J, Zhang J, Wang Z, Zhu Q, Liu LJFCR (2003) Activities of enzymes involved in sucrose-to-starch metabolism in rice grains subjected to water stress during filling. Field Crop Res 81(1):69–81
Yang J, Zhang JJNp (2006) Grain filling of cereals under soil drying. New Phytol 169(2):223–236
Yearbook CS (2019) 9. China Statistical Yearbook, National Bureau of Statistics of China. China Statistics Press, Beijing
Zhang H, Liu K, Wang Z, Liu L, Yang JJPGR (2015) Abscisic acid, ethylene and antioxidative systems in rice grains in relation with grain filling subjected to postanthesis soil-drying. Plant Growth Regul 76(2):135–146
Zhang H, Xue Y, Wang Z, Yang J, Zhang JJCS (2009) An alternate wetting and moderate soil drying regime improves root and shoot growth in rice. Crop Sci 49(6):2246–2260
Zhang H, Yu C, Kong X, Hou D, Gu J, Liu L, Wang Z, Yang JJFCR (2018) Progressive integrative crop managements increase grain yield, nitrogen use efficiency and irrigation water productivity in rice. Field Crop Res 215:1–11
Zhang Q, Liu J, Liu X, Li S, Sun Y, Lu W, Ma C (2020) Optimizing water and phosphorus management to improve hay yield and water-and phosphorus-use efficiency in alfalfa under drip irrigation. Food Sci Nutr 8(5):2406–2418
Zhang W, Liu D-Y, Li C, Chen X-P, Zou C-Q (2017a) Accumulation, partitioning, and bioavailability of micronutrients in summer maize as affected by phosphorus supply. Eur J Agron 86:48–59
Zhang X (1992) The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. Research methodology of crop physiology. Agriculture Press, Beijing, pp 208–211
Zhang Y, Liu M, Dannenmann M, Tao Y, Yao Z, Jing R, Zheng X, Butterbach-Bahl K, Lin SJFCR (2017b) Benefit of using biodegradable film on rice grain yield and N use efficiency in ground cover rice production system. Field Crop Res 201:52–59
Zhou T, Du Y, Ahmed S, Liu T, Ren M, Liu W, Yang WJFips (2016) Genotypic differences in phosphorus efficiency and the performance of physiological characteristics in response to low phosphorus stress of soybean in southwest of China. Front Plant Sci 7:1776
Funding
We greatly appreciate the financial support from the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences, Cotton Research Institute, Chinese Academy of Agricultural Sciences, State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences (Grant No.: CB2021C10), and Basic Research Service Fund of Central Public Welfare Scientific Institutions (Grant No.: 1610162021025).
Author information
Authors and Affiliations
Contributions
AI: Conceptualization, Data curation, Investigation, Methodology, Validation, Visualization, Writing—original draft, Writing—review & editing. DQ: Conceptualization, Methodology, Project administration, Resources, Software, Supervision, Writing—original draft, Writing—review & editing. WX: Data curation, Resources, Software, Visualization. GH: Formal analysis, Methodology. ZH: Data curation, Formal analysis. ZX: Funding acquisition, Project administration, Resources, Software, Supervision, Writing—review & editing. SM: Conceptualization, Funding acquisition, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing—review & editing.
Corresponding authors
Ethics declarations
Conflict of interest
All the authors declare no conflict of interest.
Additional information
Handling Editor: Jose M. Miguel.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Iqbal, A., Qiang, D., Xiangru, W. et al. Low Phosphorus Tolerance in Cotton Genotypes is Regulated by Root Morphology and Physiology. J Plant Growth Regul 42, 3677–3695 (2023). https://doi.org/10.1007/s00344-022-10829-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-022-10829-5