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Morphological, Biochemical, and Proteomic Studies Revealed Impact of Fe and P Crosstalk on Root Development in Phaseolus vulgaris L

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Abstract

Mineral stress is one of the major abiotic stresses faced by crop plants. The present study was undertaken to investigate the impact of mineral stress (iron (Fe) and phosphorus (P)) on various morphological and biochemical responses of the shoot and root tissues and root architecture of common bean (Phaseolus vulgaris L.). This study also leads us to the identification of P stress responsive proteins. The study was conducted under in vitro conditions, in which seeds of Shalimar French Bean-1 (SFB-1) variety were cultured on four different MGRL medium (control (P1Fe1), iron deficient (P1Fe0), phosphorus deficient (P0Fe1), and phosphorus and iron deficient (P0Fe0)). Chlorophyll content of leaves, Fe/P content of root tissues, total sugars, proline, length, and weight of shoot and root tissues were assessed and compared within and between the treatments. The analyzed data revealed significant difference between control and other three treatments. Chlorophyll content of shoots was found significantly decreased under mineral stress treatments P0Fe1, P1Fe0, and P0Fe0 than control. Length and weight of shoot and root were also observed significantly decreased under P0Fe1, P1Fe0, and P0Fe0 as compared to control. Total sugar was significantly higher in P0Fe1 of roots in comparison to control. Proline content was significantly higher in both tissues of shoots and roots of plants grown under P1Fe0, P0Fe1, and P0Fe0 than control condition. Furthermore, we unexpectedly observed the recovery of roots (mainly primary roots) under P0Fe0 as compared to P1Fe0 and P0Fe1. Interestingly higher concentration of Fe was also observed in P0Fe1 compared to other treatments and also higher concentration of P was observed in P1Fe1. These findings suggested that there is a crosstalk between Fe and P and also revealed that there is a disruption in the ability of PR (primary root) to sense local P deficiency in the absence of Fe. Furthermore, proteomics analysis (SDS-PAGE followed by MALDI MS) helped in identification of defensive proteins in P stress condition compared to control.

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I, the corresponding author (Sajad M Zargar), declare on behalf of all the authors that as per policy of the Journal, the data and material can be made available.

References

  1. Urwat, U., Zargar, S. M., Manzoor, M., Ahmad, S. M., Ganai, N. A., Murtaza, I., … Nehvi, F. A. (2019). Morphological and biochemical responses of Phaseolus vulgaris L. to mineral stress under in vitro conditions. Vegetos, 32(3). https://doi.org/10.1007/s42535-019-00051-2

  2. Uhde-Stone, C., Zinn, K. E., Ramirez-Yáñez, M., Li, A., Vance, C. P., & Allan, D. L. (2003). Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiology, 131(3). https://doi.org/10.1104/pp.102.016881

  3. Lynch, J. P. (2011). Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiology, 156(3). https://doi.org/10.1104/pp.111.175414

  4. Plaxton, W. C., & Tran, H. T. (2011). Metabolic adaptations of phosphate-starved plants. Plant Physiology, 156(3). https://doi.org/10.1104/pp.111.175281

  5. Van Kauwenbergh, S. J. (2010). World phosphate rock reserves and resources. Ifdc-T-75

  6. Tyagi, W., & Rai, M. (2017). Root transcriptomes of two acidic soil adapted Indica rice genotypes suggest diverse and complex mechanism of low phosphorus tolerance. Protoplasma, 254(2). https://doi.org/10.1007/s00709-016-0986-7

  7. Briat, J. F., Dubos, C., & Gaymard, F. (2015). Iron nutrition, biomass production, and plant product quality. Trends in Plant Science. https://doi.org/10.1016/j.tplants.2014.07.005

    Article  PubMed  Google Scholar 

  8. Schachtman, D. P., Reid, R. J., & Ayling, S. M. (1998). Phosphorus uptake by plants: From soil to cell. Plant Physiology. https://doi.org/10.1104/pp.116.2.447

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bonser, A. M., Lynch, J., & Snapp, S. (1996). Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytologist, 132(2). https://doi.org/10.1111/j.1469-8137.1996.tb01847.x

  10. FAOSTAT. (2018). http://www.fao.org/faostat/en/#home. Accessed 5 Apr 2021.

  11. Castro-Guerrero, N. A., Isidra-Arellano, M. C., Mendoza-Cozat, D. G., & Valdés-López, O. (2016). Common bean: A legume model on the rise for unraveling responses and adaptations to iron, zinc, and phosphate deficiencies. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2016.00600

    Article  PubMed  PubMed Central  Google Scholar 

  12. Zargar, S. M., Agrawal, G. K., Rakwal, R., & Fukao, Y. (2015). Quantitative proteomics reveals role of sugar in decreasing photosynthetic activity due to Fe deficiency. Frontiers in Plant Science, 6(AUG). https://doi.org/10.3389/fpls.2015.00592

  13. Mandre, M., Tullus, H., & Klõšeiko, J. (2002). Partitioning of carbohydrates and biomass of needles in Scots pine canopy. Zeitschrift fur Naturforschung - Section C Journal of Biosciences, 57(3–4). https://doi.org/10.1515/znc-2002-3-417

  14. Jin, Z. M., Wang, C. H., Liu, Z. P., & Gong, W. J. (2007). Physiological and ecological characters studies on Aloe vera under soil salinity and seawater irrigation. Process Biochemistry, 42(4). https://doi.org/10.1016/j.procbio.2006.11.002

  15. Huang, C. Y., Roessner, U., Eickmeier, I., Genc, Y., Callahan, D. L., Shirley, N., … Bacic, A. (2008). Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant & Cell Physiology, 49(5), 691–703. https://doi.org/10.1093/pcp/pcn044

  16. Nimir, N. E. A., & Guisheng, Z. (2018). Photosynthesis and carbon metabolism. Photosynthesis - From its evolution to future improvements in photosynthetic efficiency using nanomaterials. IntechOpen. https://doi.org/10.5772/intechopen.78031

  17. Meyer, E. H., Welchen, E., & Carrie, C. (2019). Assembly of the complexes of the oxidative phosphorylation system in land plant mitochondria. Annual Review of Plant Biology, 70(1), 23–50. https://doi.org/10.1146/annurev-arplant-050718-100412

    Article  CAS  PubMed  Google Scholar 

  18. Rout, G. R., & Sahoo, S. (2015). Role of iron in plant growth and metabolism. Reviews in Agricultural Science, 3, 1–24. https://doi.org/10.7831/ras.3.1

    Article  Google Scholar 

  19. Liao, H., Rubio, G., Yan, X., Cao, A., Brown, K. M., & Lynch, J. P. (2001). Effect of phosphorus availability on basal root shallowness in common bean. Plant and Soil, 232(1–2). https://doi.org/10.1023/A:1010381919003

  20. Liao, H., Yan, X., Rubio, G., Beebe, S. E., Blair, M. W., & Lynch, J. P. (2004). Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Functional Plant Biology, 31(10). https://doi.org/10.1071/FP03255

  21. Lynch, J., Läuchli, A., & Epstein, E. (1991). Vegetative growth of the common bean in response to phosphorus nutrition. Crop Science, 31(2). https://doi.org/10.2135/cropsci1991.0011183x003100020031x

  22. Beebe, S. E., Rojas-Pierce, M., Yan, X., Blair, M. W., Pedraza, F., Muñoz, F., … Lynch, J. P. (2006). Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Science, 46(1). https://doi.org/10.2135/cropsci2005.0226

  23. Yan, X., Liao, H., Beebe, S. E., Blair, M. W., & Lynch, J. P. (2004). QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant and Soil, 265(1–2). https://doi.org/10.1007/s11104-005-0693-1

  24. Zhou, J., Zhang, Z., Zhang, Y., Wei, Y., & Jiang, Z. (2018). Effects of lead stress on the growth, physiology, and cellular structure of privet seedlings. PLoS ONE, 13(3). https://doi.org/10.1371/journal.pone.0191139

  25. Bocchini, M., Bartucca, M. L., Ciancaleoni, S., Mimmo, T., Cesco, S., Pii, Y., … Del Buono, D. (2015). Iron deficiency in barley plants: Phytosiderophore release, iron translocation, and DNA methylation. Frontiers in Plant Science, 6(JULY). https://doi.org/10.3389/fpls.2015.00514

  26. Sharma, P., & Dubey, R. S. (2005). Lead toxicity in plants. Brazilian Journal of Plant Physiology. https://doi.org/10.1590/s1677-04202005000100004

    Article  Google Scholar 

  27. Sbai, H. (2018). Responses of two Apiaceae species to direct iron deficiency. International Journal of Photochemistry and Photobiology, 2(1). https://doi.org/10.11648/j.ijpp.20180201.14

  28. Zocchi, G., De Nisi, P., Dell’Orto, M., Espen, L., & Gallina, P. M. (2007). Iron deficiency differently affects metabolic responses in soybean roots. Journal of Experimental Botany, 58(5). https://doi.org/10.1093/jxb/erl259

  29. Houmani, H., Jelali, N., Abdelly, C., & Gharsalli, M. (2012). Mineral elements bioavailability in the halophyte species Suaeda fruticosa. Journal of Biological Research, 17.

  30. Molassiotis, A., Tanou, G., Diamantidis, G., Patakas, A., & Therios, I. (2006). Effects of 4-month Fe deficiency exposure on Fe reduction mechanism, photosynthetic gas exchange, chlorophyll fluorescence and antioxidant defense in two peach rootstocks differing in Fe deficiency tolerance. Journal of Plant Physiology, 163(2). https://doi.org/10.1016/j.jplph.2004.11.016

  31. Weisany, W., Sohrabi, Y., Heidari, G., Siosemardeh, A., & Kazem, G. G. (2011). Physiological responses of soybean (Glycine max L.) to zinc application under salinity stress. Australian Journal of Crop Science, 5(11).

  32. Hasaneen, M. N. A., Younis, M. E., & Tourky, S. M. N. (2009). Plant growth, metabolism and adaptation in relation to stress conditions XXIII. Salinity-biofertility interactive effects on growth, carbohydrates and photosynthetic efficiency of Lactucasativa. Plant Omics Journal Southern Cross Journals©2009, 2(2), 60–69.

    CAS  Google Scholar 

  33. Mahmoudi, H., Labidi, N., Ksouri, R., Gharsalli, M., & Abdelly, C. (2007). Differential tolerance to iron deficiency of chickpea varieties and Fe resupply effects. Comptes Rendus - Biologies, 330(3), 237–246. https://doi.org/10.1016/j.crvi.2007.02.007

    Article  CAS  PubMed  Google Scholar 

  34. Jelali, N., Dell’Orto, M., Rabhi, M., Zocchi, G., Abdelly, C., & Gharsalli, M. (2010). Physiological and biochemical responses for two cultivars of Pisum sativum (“Merveille de Kelvedon” and “Lincoln”) to iron deficiency conditions. Scientia Horticulturae, 124(1). https://doi.org/10.1016/j.scienta.2009.12.010

  35. BAVARESCO, L., FREGONI, M., & PERINO, A. (1995). Physiological aspects of lime-induced chlorosis in some Vitis species. II: Genotype response to stress conditions. Vitis, 34(4).

  36. Sami, F., Yusuf, M., Faizan, M., Faraz, A., & Hayat, S. (2016). Role of sugars under abiotic stress. Plant Physiology and Biochemistry. https://doi.org/10.1016/j.plaphy.2016.09.005

    Article  PubMed  Google Scholar 

  37. Urwat, U., Zargar, S. M., Ahmad, S. M., & Ganai, N. A. (2021). Insights into role of STP13 in sugar driven signaling that leads to decrease in photosynthesis in dicot legume crop model (Phaseolus vulgaris L.) under Fe and Zn stress. Molecular Biology Reports. https://doi.org/10.1007/s11033-021-06295-z

  38. Sandhya, V., Ali, S. Z., Grover, M., Reddy, G., & Venkateswarlu, B. (2010). Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regulation, 62(1). https://doi.org/10.1007/s10725-010-9479-4

  39. Lin, X. Y., Ye, Y. Q., Fan, S. K., Jin, C. W., & Zheng, S. J. (2016). Increased sucrose accumulation regulates iron-deficiency responses by promoting auxin signaling in Arabidopsis plants. Plant Physiology, 170(2). https://doi.org/10.1104/pp.15.01598

  40. Amirjani, M. R. (2011). Effect of Salinity stress on growth, sugar content, pigments and enzyme activity of rice. International Journal of Botany, 7(1). https://doi.org/10.3923/ijb.2011.73.81

  41. Chen, Y. X., He, Y. F., Luo, Y. M., Yu, Y. L., Lin, Q., & Wong, M. H. (2003). Physiological mechanism of plant roots exposed to cadmium. Chemosphere, 50(6). https://doi.org/10.1016/S0045-6535(02)00220-5

  42. Arias-Baldrich, C., Bosch, N., Begines, D., Feria, A. B., Monreal, J. A., & García-Mauriño, S. (2015). Proline synthesis in barley under iron deficiency and salinity. Journal of Plant Physiology, 183. https://doi.org/10.1016/j.jplph.2015.05.016

  43. Meng, X., Chen, W. W., Wang, Y. Y., Huang, Z. R., Ye, X., Chen, L. S., & Yang, L. T. (2021). Effects of phosphorus deficiency on the absorption of mineral nutrients, photosynthetic system performance and antioxidant metabolism in Citrus grandis. PLoS ONE, 16(2 February). https://doi.org/10.1371/journal.pone.0246944

  44. Hirsch, J., Marin, E., Floriani, M., Chiarenza, S., Richaud, P., Nussaume, L., & Thibaud, M. C. (2006). Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie, 88(11). https://doi.org/10.1016/j.biochi.2006.05.007

  45. Pieters, A. J., Paul, M. J., & Lawlor, D. W. (2001). Low sink demand limits photosynthesis under P(i) deficiency. Journal of Experimental Botany, 52(358), 1083–1091. https://doi.org/10.1093/jexbot/52.358.1083

    Article  CAS  PubMed  Google Scholar 

  46. Rai, V., Sanagala, R., Sinilal, B., Yadav, S., Sarkar, A. K., Dantu, P. K., & Jain, A. (2014). Iron availability affects phosphate deficiency-mediated responses, and evidence of cross-talk with auxin and zinc in arabidopsis. Plant and Cell Physiology, 56(6). https://doi.org/10.1093/pcp/pcv035

  47. Svistoonoff, S., Creff, A., Reymond, M., Sigoillot-Claude, C., Ricaud, L., Blanchet, A., … Desnos, T. (2007). Root tip contact with low-phosphate media reprograms plant root architecture. Nature Genetics, 39(6). https://doi.org/10.1038/ng2041

  48. Ward, J. T., Lahner, B., Yakubova, E., Salt, D. E., & Raghothama, K. G. (2008). The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiology, 147(3). https://doi.org/10.1104/pp.108.118562

  49. Zhao, H., Yang, A., Kong, L., Xie, F., Wang, H., & Ao, X. (2021). Proteome characterization of two contrasting soybean genotypes in response to different phosphorus treatments. AoB PLANTS, 13(3), plab019. https://doi.org/10.1093/aobpla/plab019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zheng, L., Huang, F., Narsai, R., Wu, J., Giraud, E., He, F., … Shou, H. (2009). Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiology, 151(1). https://doi.org/10.1104/pp.109.141051

  51. Opassiri, R., Pomthong, B., Akiyama, T., Nakphaichit, M., Onkoksoong, T., Ketudat Cairns, M., & Ketudat Cairns, J. R. (2007). A stress-induced rice (Oryza sativa L.) β-glucosidase represents a new subfamily of glycosyl hydrolase family 5 containing a fascin-like domain. Biochemical Journal, 408(2). https://doi.org/10.1042/BJ20070734

  52. Meirinho, S., Carvalho, M., Dominguez, Á., & Choupina, A. (2010). Isolation and characterization by asymmetric PCR of the ENDO1 gene for glucan endo-1,3-β-D-glucosidase in phytophthora cinnamomi associated with the ink disease of Castanea sativa Mill. Brazilian Archives of Biology and Technology, 53(3). https://doi.org/10.1590/S1516-89132010000300003

  53. Staswick, P. E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M. T., Maldonado, M. C., & Suza, W. (2005). Characterization of an arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell, 17(2). https://doi.org/10.1105/tpc.104.026690

  54. Feng, S., Yue, R., Tao, S., Yang, Y., Zhang, L., Xu, M., … Shen, C. (2015). Genome-wide identification, expression analysis of auxin-responsive GH3 family genes in maize (Zea mays L.) under abiotic stresses. Journal of Integrative Plant Biology, 57(9). https://doi.org/10.1111/jipb.12327

  55. Domingo, C., Andrés, F., Tharreau, D., Iglesias, D. J., & Talón, M. (2009). Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Molecular Plant-Microbe Interactions, 22(2). https://doi.org/10.1094/MPMI-22-2-0201

  56. Zhang, S. W., Li, C. H., Cao, J., Zhang, Y. C., Zhang, S. Q., Xia, Y. F., … Sun, Y. (2009). Altered architecture and enhanced drought tolerance in rice via the down-regulation of Indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiology, 151(4). https://doi.org/10.1104/pp.109.146803

  57. Du, H., Wu, N., Fu, J., Wang, S., Li, X., Xiao, J., & Xiong, L. (2012). A GH3 family member, OsGH3–2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. Journal of Experimental Botany, 63(18). https://doi.org/10.1093/jxb/ers300

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Funding

Sajad Majeed Zargar acknowledges NMHS GBPNIHESD, Almora, Uttrakhand, India, for partial financial support of the research on Common bean (Project Sanction Order No. GBPNI/NMHS17-18/SG24/622).

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Authors and Affiliations

  1. Proteomics Laboratory, Division of Plant Biotechnology, Sher-E-Kashmir University of Agricultural Sciences & Technology of Kashmir, Shalimar, Srinagar, Jammu & Kashmir, India, 190025

    Madhiya Manzoor, Sajad Majeed Zargar, Parveen Akhter, Uneeb Urwat & Reetika Mahajan

  2. Division of Basic Science, Sher-E-Kashmir University of Agricultural Sciences & Technology of Kashmir, Shalimar, Srinagar, Jammu & Kashmir, India

    Sajad Ahmad Bhat

  3. Department of Clinical Biochemistry, University of Kashmir, Hazratbal, Srinagar, Jammu & Kashmir, India

    Tanveer Ali Dar

  4. Division of Agricultural Statistics, Sher-E-Kashmir University of Agricultural Sciences & Technology of Kashmir, Shalimar, Srinagar, Jammu & Kashmir, India

    Imran Khan

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  1. Madhiya Manzoor
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Contributions

Madhiya Manzoor did experimental work and helped in preparing the draft; Sajad Majeed Zargar developed the concept and guided all the research work and helped in finalizing of manuscript and in revising the manuscript; Parveen Akhter did shoot proteome analysis; Uneeb Urwat did data analysis; Sajad Ahmad Bhat guided in taking physiological observations; Reetika Mahajan helped in proteome data analysis and preparing the manuscript and in revision; Tanveer Ali Dar guided in biochemical analysis and its discussion; Imran Khan helped in statistical analysis of physiological, biochemical, and morphological data.

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Correspondence to Sajad Majeed Zargar.

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Manzoor, M., Zargar, S.M., Akhter, P. et al. Morphological, Biochemical, and Proteomic Studies Revealed Impact of Fe and P Crosstalk on Root Development in Phaseolus vulgaris L. Appl Biochem Biotechnol 193, 3898–3914 (2021). https://doi.org/10.1007/s12010-021-03662-1

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