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Impact of phosphorous-deficit conditions on morpho-physiological traits and phosphorous metabolism in chickpea genotypes

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Abstract

Chickpea, an important food legume, is primarily grown on marginal soils with low soil fertility. Although chickpea can fix N, soil phosphorus (P) deficiency in crop growing areas is a major limiting factor for chickpea production. This study was undertaken to evaluate twenty-five chickpea cultivars for morpho-physiological traits and yield under low and normal phosphorous conditions. Based on morpho-physiological traits such as length and area of roots and shoots, root length density, root and shoot biomass, chlorophyll content, number of nodules and root tips, tolerance indices and yield, these cultivars were characterised into susceptible (ICC67, ICC1915, ICC2593, ICC5337, ICC5879, ICC8950, ICC13441, ICC1483, ICC15606 and ICC15888), tolerant (ICC10755, IG72070, ICCV97105, ICCV2, ICCV92809, ICCV92337 and ICCV95423) and the remaining cultivars were moderately tolerant to phosphorous-deficit conditions. Higher activities of enzymes of phosphorous metabolism such as acid phosphatase and phytase in roots and nodules of tolerant chickpea cultivars (ICCV97105, ICCV92337, ICCV95423) as compared to susceptible cultivars (ICC67, ICC15606, ICC15888) at different developmental stages might be attributing to their better performance for growth parameters and productivity traits under phosphorous-deficit conditions.

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References

  • Abadia J, Rao IM, Terry N (1987) Changes in leaf phosphate status have only small effects on the photochemical apparatus of sugar beet leaves. Plant Sci 50:49–55

    Article  CAS  Google Scholar 

  • Ames B (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8:115–118

    Article  CAS  Google Scholar 

  • Araújo AP, Plassard C, Drevon JJ (2008) Phosphatase and phytase activities in nodules of common bean genotypes at different levels of phosphorous supply. Plant Soil 312:129–138

    Article  CAS  Google Scholar 

  • Aziz T, Sabir M, Farooq M, Maqsood MA, Ahmad HR, Warraich EA (2014) Phosphorous deficiency in plants: responses, adaptive mechanisms, and signaling. In: Hakeem KR, Rehman RU, Tahir I (eds.) Plant signaling: understanding the molecular crosstalk. Springer, pp 355. https://doi.org/10.1007/978-81-322-1542-4_7

  • Brown KM (2001) Topsoil foraging: an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–323

    Article  Google Scholar 

  • Cabeza RA, Liese R, Lingner A, Stieglitz I, Neumann J, Salinas-Riester G, Pommerenke C, Dittert K, Schulze J (2014) RNA-seq transcriptome profiling reveals that Medicago truncatula nodules acclimate N2 -fixation before emerging P deficiency reaches the nodules. J Exp Bot 65:6035–6048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camacho-Cristóbal JJ, Rexach J, Conéjéro G, Al-Ghazi Y, Nacry P, Doumas P (2008) PRD, an Arabidopsis AINTEGUMENTA-like gene, is involved in root architectural changes in response to phosphate starvation. Planta 228:511–522

    Article  CAS  PubMed  Google Scholar 

  • Cheema HS, Singh B (1991) Software statistical CPCS-1. Department of Statistics, Punjab Agricultural University, Ludhiana, India, Ludhiana

    Google Scholar 

  • de Groot BL, Grubmüller H (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Sci 294:2353–2357

    Article  Google Scholar 

  • Deng Y, Men C, Qiao S, Wang W, Gu J, Liu L, Zhang Z, Zhang H, Wang Z, Yang J (2020) Tolerance to low phosphorous in rice varieties is conferred by regulation of root growth. Crop J 8:534–47

    Article  Google Scholar 

  • Dhillon GS, Das N, Kaur S, Srivastava P, Bains NS, Chhuneja P (2021) Marker assisted mobilization of heat tolerance QTLs from Triticum durum-Aegilops speltoides introgression lines to hexaploid wheat. Indian J Genet 81(2):186–198

    CAS  Google Scholar 

  • Divito GA, Sadras VO (2014) How do phosphorous, potassium and sulphur affect plant growth and biological nitrogen fixation in crop and pasture legumes? A meta-analysis. Field Crops Res 156:161–171

    Article  Google Scholar 

  • FAOSTAT (2019) Food and Agriculture Organisation of United Nations (FAO) Statistical Databases. http://faostat.fao.org

  • FAOSTAT (2020) Food and Agriculture Organisation of United Nations (FAO) Statistical Databases. http://faostat.fao.org

  • Farah N, Nosheen S (2006) Effect of phosphorous application on the growth and nodulation of inoculated chickpea (Cicer arietinum L.). Pak J Agric Sci Res 19(4):65–69

    Google Scholar 

  • Flugge UI, Heldt HW (1984) The phosphate-triose phosphate-phosphoglycerate translocator of the chloroplast. Trends Biochem Sci 9(12):530–533

    Article  Google Scholar 

  • Gniazdowska A, Mikulska M, Rychter AM (1998) Growth, nitrate uptake and respiration rate in bean roots under phosphate deficiency. Biol Plant 41:217–226

    Article  CAS  Google Scholar 

  • Gopalan C, Rama Sastri BV, Balasubramanian SC (2012) Nutritive value of Indian foods. National Institute of Nutrition, Indian Council of Medical Research, Hyderabad

  • Halsted M, Lynch J (1996) Phosphorous responses of C3 and C4 species. J Exp Bot 47:497–505

    Article  CAS  Google Scholar 

  • Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617

    Article  CAS  PubMed  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    Article  CAS  Google Scholar 

  • Jackson ML (1973) Soil chemical analysis - advanced course a manual of methods useful for instruction and research in soil chemistry, physical chemistry of soils, soil fertility, and soil genesis. Madison, Wisconsin (Publisher) Published by the author, Department of Science, University of Wisconsin (2nd edition)

  • Jeschke WD, Kirkby EA, Peuke AD, Pate JS, Hartung W (1997) Effects of P deficiency on assimilation and transport of nitrate and phosphate in intact plants of castor bean (Ricinus communis L.). J Exp Bot 48(1):75–91

    Article  CAS  Google Scholar 

  • Jukanti AK, Gaur PM, Gowda CL, Chibbar RN (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Brit J Nutr 108(Suppl 1):S11–S26. https://doi.org/10.1017/S0007114512000797

    Article  CAS  PubMed  Google Scholar 

  • Kouas S, Louche J, Debez A, Plassard C, Drevon JJ, Abdelly C (2009) Effect of phosphorous deficiency on acid phosphatase and phytase activities in common bean (Phaseolus vulgaris L.) under symbiotic nitrogen fixation. Symbiosis 47:141–149. https://doi.org/10.1007/BF03179974

    Article  CAS  Google Scholar 

  • Lai F, Thacker J, Li Y, Doerner P (2007) Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J 50:545–556

    Article  CAS  PubMed  Google Scholar 

  • Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorous: matching morphological and physiological traits. Ann Bot 98:693–713

    Article  PubMed  PubMed Central  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. https://doi.org/10.1016/j.tree.2007.10.008

    Article  PubMed  Google Scholar 

  • Lambers H, Brundrett M, Raven J, Hopper S (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31

    Article  CAS  Google Scholar 

  • Lazali M, Brahimi S, Merabet C, Latati MC, Benadis C, Maougal RT, Blavet D, Drevon JJ, Ounane SM (2016) Nodular diagnosis of contrasting recombinant inbred lines of Phaseolus vulgaris in multi-local field tests under Mediterranean climate. Eur J Soil Biol 73:100–07. https://doi.org/10.1016/j.ejsobi.2016.02.002

    Article  CAS  Google Scholar 

  • Liu H, Tang C, Li C (2016) The effects of nitrogen form on root morphological and physiological adaptations of maize, white lupin and faba bean under phosphorous deficiency. AoB Plants 8:lw058. https://doi.org/10.1093/aobpla/plw058

  • Lopez-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129(1):244–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma XF, Wright E, Ge Y, Bell J, Xi Y, Bouton JH, Wang ZY (2009) Improving phosphorous acquisition of white clover (Trifolium repens L.) by transgenic expression of plant-derived phytase and acid phosphatase genes. Plant Sci 176:479–488

    Article  CAS  PubMed  Google Scholar 

  • Martins D, Macovei A, Leonetti P, Balestrazzi A, Araújo S (2017) The influence of phosphate deficiency on legume symbiotic N2 fixation. In: Sulieman S, Tran LS (eds) Legume nitrogen fixation in soils with low phosphorus availability. Springer, Cham

    Google Scholar 

  • Midekssa MJ, Löscher CR, Schmitz RA, Assefa F (2016) Phosphate solubilization and multiple plant growth promoting properties of rhizobacteria isolated from chickpea (Cicer aeritinum L.) producing areas of Ethiopia. Afr J Biotechnol 15:1899–1912

    Article  CAS  Google Scholar 

  • Mitran T, Mani PK (2017) Effect of organic amendments on rice yield trend, phosphorous use efficiency, uptake, and apparent balance in soil under long-term rice-wheat rotation. J Plant Nutr 40(9):1312–1322

    Article  CAS  Google Scholar 

  • Mollier A, Pellerin S (1999) Maize root system growth and development as influenced by phosphorous deficiency. J Exp Bot 50:487–497

    Article  CAS  Google Scholar 

  • Mudge SR, Smith FW, Richardson AE (2003) Root-specific and phosphate-regulated expression of phytase under the control of a phosphate transporter promoter enables Arabidopsis to grow on phytate as a sole P source. Plant Sci 165:871–878

    Article  CAS  Google Scholar 

  • Nesme T, Colomb B, Hinsinger P, Watson CA (2014) Soil phosphorus management in organic cropping systems: from current practices to avenues for a more efficient use of P resources. Organic farming, prototype for sustainable agricultures. Springer, Berlin, pp 23–45

    Chapter  Google Scholar 

  • Nguyen VL, Palmer L, Roessner U, Stangoulis J (2019) Genotypic variation in the root and shoot metabolite profiles of wheat (Triticum aestivum L.) indicate sustained, preferential carbon allocation as a potential mechanism in phosphorous efficiency. Front Plant Sci 10:995

    Article  PubMed  PubMed Central  Google Scholar 

  • Niu Y, Chai R, Jin G, Wang H, Tang C, Zhang Y (2012) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nole-Wilson S, Tranby TL, Krizek BA (2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol 57:613–628

    Article  CAS  PubMed  Google Scholar 

  • Olaleye O, Olajire F, Nnenna I (2011) Phosphorus response efficiency in Cowpea genotypes. J Agric Sci 4:81. https://doi.org/10.5539/jas.v4n1p81

    Article  Google Scholar 

  • Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KH (2018) The carboxylate-releasing phosphorous-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorous supply. New Phytol 219:518–529

    Article  CAS  PubMed  Google Scholar 

  • Piper CS (1942) Soil and plant analysis: a laboratory manual of methods for the examination of soils and the determination of the inorganic constituents of plants. University of Adelaide, Adelaide, pp 368

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  CAS  PubMed  Google Scholar 

  • Rao IM, Terry N (1989) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet: I. Changes in growth, gas exchange, and Calvin cycle enzymes. Plant Physiol 90:814–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasool S, Abdel Latef AA, Ahmad P (2015) Chickpea. In: Azooz MM, Ahmad P (eds) Legumes under environmental stress. Wiley, Chichester

    Google Scholar 

  • Reddy VRP, Das S, Dikshit HK, Mishra GP, Aski M, Meena SK et al (2020) Genome-wide association analysis for phosphorus use efficiency traits in mungbean (Vigna radiata L. Wilczek) using genotyping by sequencing approach. Front Plant Sci 11:537766

    Article  PubMed  PubMed Central  Google Scholar 

  • Rengel Z (2001) Genotypic differences in micronutrient use efficiency in crops. Commun Soil Sci Plant Anal 32(7–8):1163–1186

    Article  CAS  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906

    Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156

    Article  CAS  Google Scholar 

  • Rotaru V, Sinclair TR (2009) Interactive influence of phosphorus and iron on nitrogen fixation by soybean. Environ Exp Bot 66(1):94–99

    Article  CAS  Google Scholar 

  • Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L (2006) Characterization of low phosphorous insensitive mutants reveals a crosstalk between low phosphorous-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorous deficiency. Plant Physiol 140:879–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulze J, Temple G, Temple SJ, Beschow H, Vance CP (2006) Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot 98:731–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh B, Satyanarayana (2011) Microbial phytases in phosphorous acquisition and plant growth promotion. Physiol Mol Biol Plants 17:93–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh N, Singh G (2016) Response of lentil (Lens culinaris Medikus) to phosphorous-a review. Agric Rev 37(1):27–34

    CAS  Google Scholar 

  • Singh U, Singh B (2014) Effect of basal and foliar application of diammonium phosphate in cognizance with phosphate-solubilizing bacteria on growth, yield and quality of rainfed chickpea (Cicer arietinum). Indian J Agron 59(3):427–432

    Google Scholar 

  • Srinivasarao C, Ganeshamurthy AN, Ali M, Venkateswarlu B (2006) Phosphorous and micronutrient nutrition of chickpea genotypes in a multi-nutrient-deficient typic ustochrept. J Plant Nutr 29:747–763

    Article  CAS  Google Scholar 

  • Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39(6):792–796

    Article  CAS  PubMed  Google Scholar 

  • Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775–789

    Article  CAS  PubMed  Google Scholar 

  • Thuynsma R, Valentine A, Kleinert A (2014) Phosphorus deficiency affects the allocation of below-ground resources to combined cluster roots and nodules. Lupinus Albus. J Plant Physiol 171:285–291. https://doi.org/10.1016/j.jplph.2013.09.001

    Article  CAS  PubMed  Google Scholar 

  • Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37:801–814

    Article  CAS  PubMed  Google Scholar 

  • Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805

    Article  CAS  PubMed  Google Scholar 

  • Valentine A, Osborne B, Mitchell D (2001) Interactions between phosphorus supply and total nutrient availability on mycorrhizal colonization, growth and photosynthesis of cucumber. Sci Hort 88:177–189

    Article  CAS  Google Scholar 

  • van de Wiel CC, van der Linden CG, Scholten OE (2016) Improving phosphorous use efficiency in agriculture: opportunities for breeding. Euphytica 207(1):1–22

    Article  Google Scholar 

  • Veronica N, Subrahmanyam D, Kiran TV, Yugandhar P, Bhadana VP, Padma V, Jayasree G, Voleti SR (2017) Influence of low phosphorous concentration on leaf photosynthetic characteristics and antioxidant response of rice genotypes. Photosynthetica 55:285–293

    Article  CAS  Google Scholar 

  • Wang X, Shen J, Liao H (2010) Acquisition or utilization, which is more critical for enhancing phosphorous efficiency in modern crops? Plant Sci 179(4):302–306

    Article  CAS  Google Scholar 

  • Wang X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Lu J, Yang M, Yang H, Zhang Q (2015) Stoichiometric characteristics of carbon, nitrogen, and phosphorous in leaves of differently aged lucerne (Medicago sativa) stands. Front Plant Sci 6:1062

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang YS, Jensen LS, Magid J (2016) Differential responses of root and root hair traits of spring wheat genotypes to phosphorous deficiency in solution culture. Plant Soil Environ 62:540–546

    Article  CAS  Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York, pp 1–260

    Book  Google Scholar 

  • Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265(1):17–29

    Article  CAS  Google Scholar 

  • Zhu J, Zhang C, Lynch JP (2010) The utility of phenotypic plasticity of root hair length for phosphorous acquisition. Funct Plant Biol 37(4):313–322

    Article  Google Scholar 

  • Zhu CQ, Zhu XF, Hu AY, Wang C, Wang B, Dong XY, Shen RF (2016) Differential effects of nitrogen forms on cell wall phosphorus remobilization are mediated by nitric oxide, pectin content, and phosphate transporter expression. Plant Physiol 171:1407–1417

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Pulses Section, Department of Plant Breeding and Genetics, Punjab Agricultural University, Ludhiana for providing seeds and field for sowing of crop.

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  1. Department of Biochemistry, Punjab Agricultural University, Ludhiana, 141004, India

    Suchint Kaur & Satvir Kaur Grewal

  2. Department of Plant Breeding and Genetics, Punjab Agricultural University, Ludhiana, 141004, India

    Sarvjeet Singh & Harpreet Kaur Virk

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  1. Suchint Kaur
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  4. Harpreet Kaur Virk
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Suchint Kaur: methodology, formal analysis, investigation, data curation writing—original draft. Satvir Kaur Grewal: conceptualization, supervision, resources, writing, review and editing. Sarvjeet Singh: conceptualization, resources, review and editing. Harpreet Kaur Virk: investigation, review and editing.

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Kaur, S., Grewal, S.K., Singh, S. et al. Impact of phosphorous-deficit conditions on morpho-physiological traits and phosphorous metabolism in chickpea genotypes. Protoplasma 259, 775–788 (2022). https://doi.org/10.1007/s00709-021-01700-7

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