The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Physiological and Biochemical Changes in Lucerne (Medicago sativa) Plants Infected with 'Candidatus Phytoplasma australasia'-Related Strain (16SrII-D Subgroup)

  • Ayvaci, Humeyra (Department of Plant Protection, Faculty of Agriculture, Harran University) ;
  • Guldur, M. Ertugrul (Department of Plant Protection, Faculty of Agriculture, Harran University) ;
  • Dikilitas, Murat (Department of Plant Protection, Faculty of Agriculture, Harran University)
  • Received : 2021.12.28
  • Accepted : 2022.03.10
  • Published : 2022.04.01
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Abstract

Changes in physiological and biochemical patterns in lucerne plants caused by the presence of 'Candidatus Phytoplasma australasia', which is one of the significant pathogens causing yield losses in lucerne plants, were investigated. Significant differences were evident in total chlorophyll, chlorophyll a, chlorophyll b, and protein amounts between 'Ca. Phytoplasma australasia'-positive and negative lucerne plants. Stress-related metabolites such as phenol, malondialdehyde, and proline accumulations in 'Ca. Phytoplasma australasia'-positive plants were remarkably higher than those of phytoplasma-negative plants. As a response to disease attack, phytoplasma-positive plants exhibited higher antioxidant enzymes (peroxidase and catalase) and nonenzymatic metabolite responses such as jasmonic and salicylic acids. We state that partial disease responses were revealed for the first time to breed resistant lucerne lines infected by 'Ca. Phytoplasma australasia'.

Keywords

Acknowledgement

The first author expresses her gratitude the their education YOK (Phd 100-2000) and Harran University for support a bursary.

References

  1. Acikbas, S., Albayrak, S. and Turk, M. 2017. Determination of forage yield and quality of some alfalfa (Medicago sativa L.) genotypes collected from natural vegetation. Turk. J. Agric. Res. 4:155-162.
  2. Ahmad, D., Jain, S. K., Joshi, M. A., Anand, A., Tomar, B. S., Kumar, S. and Hasan, M. 2021. H2O2 as a better index of seed quality and mechanism of cucumber (Cucumis sativus) seed deterioration. Indian J. Agric. Sci. 91:1500-1504.
  3. Ahrens, U. and Seemuller, E. 1992. Detection of DNA of plant pathogenic mycoplasmalike organisms by a polymerase chain reaction that amplifies a sequence of the 16S rRNA gene. Phytopathology 82:828-832. https://doi.org/10.1094/Phyto-82-828
  4. Alcicek, A. 2002. Basic principles in making dairy cattle ration. Aegean Agric. Res. Inst. Publ. 106:124-135.
  5. Annigeri, S., Pankaj, Shakil, N. A., Kumar, J. and Singh, K. 2011. Effect of jasmonate (jasmonic acid) foliar spray on resistance in tomato infected with root-knot nematode, Meloidogyne incognita. Ann. Plant Prot. Sci. 19:446-450.
  6. Arce-Leal, A. P., Bautista, R., Rodriguez-Negrete, E. A., Manzanilla- Ramirez, M. A., Velazquez-Monreal, J. J., Santos-Cervantes, M. E., Mendez-Lozano, J., Beuzon, C. R., Bejarano, E. R., Castillo, A. G., Claros, M. G. and Leyva-Lopez, N. E. 2020. Gene expression profile of Mexican lime (Citrus aurantifolia) trees in response to Huanglongbing disease caused by Candidatus Liberibacter asiaticus. Microorganisms 8:528. https://doi.org/10.3390/microorganisms8040528
  7. Arnon, D. L. 1949. Copper enzyme is isolated chloroplast: polyphenol oxidase in Beta vulgaries. Plant Physiol. 24:1-15. https://doi.org/10.1104/pp.24.1.1
  8. Ayvaci, H., Guldur, M. E., Simsek, E. and Dikilitas, M. 2020. First report of a 'Candidatus Phytoplasma australasia'-related strain (16SrII-D subgroup) associated with alfalfa leaf chlorosis disease in Turkey. New Dis. Rep. 42:20. https://doi.org/10.5197/j.2044-0588.2020.042.020
  9. Ayvaci, H., Simsek, E., Akkurak, H., Dikilitas, M. and Guldur, M. E. 2021. First report of a 'Candidatus Phytoplasma aurantifolia'-related strain associated with Cactus witches' broom disease in Opuntia sp. in Turkey. New Dis. Rep. 44:e12031.
  10. Bates, L. S., Waldren, R. P. and Teare, I. D. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39:205-207. https://doi.org/10.1007/BF00018060
  11. Bendix, C. and Lewis, J. D. 2018. The enemy within: phloemlimited pathogens. Mol. Plant Pathol. 19:238-254. https://doi.org/10.1111/mpp.12526
  12. Bernardo, L., Carletti, P., Badeck, F. W., Rizza, F., Morcia, C., Ghizzoni, R., Rouphael, Y., Colla, G., Terzi, V. and Lucini, L. 2019. Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol. Biochem. 137:203-212. https://doi.org/10.1016/j.plaphy.2019.02.007
  13. Bertamini, M., Grando, M. S. and Nedunchezhian, N. 2003. Effects of phytoplasma infection on pigments, chlorophyllprotein complex and photosynthetic activities in field grown apple leaves. Biol. Plant. 46:237-242. https://doi.org/10.1023/B:BIOP.0000022258.49957.9a
  14. Bertamini, M., Muthuchelian, K. and Nedunchezhian, N. 2004. Effect of grapevine leafroll on the photosynthesis of field grown grapevine plants (Vitis vinifera L. cv. Lagrein). J. Phytopathol. 152:145-152. https://doi.org/10.1111/j.1439-0434.2004.00815.x
  15. Boex-Fontvieille, E., Daventure, M., Jossier, M., Zivy, M., Hodges, M. and Tcherkez, G. 2013. Photosynthetic control of Arabidopsis leaf cytoplasmic translation initiation by protein phosphorylation. PLoS ONE 8:e70692. https://doi.org/10.1371/journal.pone.0070692
  16. Buoso, S., Pagliari, L., Musetti, R., Martini, M., Marroni, F., Schmidt, W. and Santi, S. 2019. 'Candidatus Phytoplasma solani' interferes with the distribution and uptake of iron in tomato. BMC Genomics 20:703. https://doi.org/10.1186/s12864-019-6062-x
  17. Chang, C. J. 1977. Histological investigation on phyllody in Catharanthus roseus. M.S. thesis. Missouri University, Columbia, MO, USA.
  18. Costarelli, A., Bianchet, C., Ederli, L., Salerno, G., Piersanti, S., Rebora, M. and Pasqualini, S. 2020. Salicylic acid induced by herbivore feeding antagonizes jasmonic acid mediated plant defenses against insect attack. Plant Signal. Behav. 15:1704517. https://doi.org/10.1080/15592324.2019.1704517
  19. Cvikorova, M., Hrubcova, M., Vagner, M., Machackova, I. and Eder, J. 1994. Phenolic acids and peroxidase activity in alfalfa (Medicago sativa) embryogenic cultures after ethephon treatment. Physiol. Plant. 91:226-233. https://doi.org/10.1034/j.1399-3054.1994.910214.x
  20. Davis, R. E. and Lee, I.-M. 1993. Cluster-specific polymerase chain reaction amplification of 16S rDNA sequences for detection and identification of mycoplasmalike organisms. Phytopathology 83:1008-1011. https://doi.org/10.1094/Phyto-83-1008
  21. de Freitas, P. A. F., de Carvalho, H. H., Costa, J. H., de Souza Miranda, R., da Cruz Saraiva, K. D., de Oliveira, F. D. B., Gomes Filho, D., Prisco, J. T. and Gomes-Filho, E. 2019. Salt acclimation in sorghum plants by exogenous proline: physiological and biochemical changes and regulation of proline metabolism. Plant Cell Rep. 38:403-416. https://doi.org/10.1007/s00299-019-02382-5
  22. Dempsey, D. A and Klessig, D. F. 2012. SOS: too many signals for systemic acquired resistance? Trends Plant Sci. 17:538-545. https://doi.org/10.1016/j.tplants.2012.05.011
  23. de Oliveira, E., Magalhaes, P. C., Gomide, R. L., Vasconcelos, C. A., Souza, I. R. P., Oliveira, C. M., Cruz, I. and Schaffert, R. E. 2002. Growth and nutrition of mollicute-infected maize. Plant Dis. 86:945-949. https://doi.org/10.1094/pdis.2002.86.9.945
  24. Derksen, H., Rampitsch, C. and Daayf, F. 2013. Signalling crosstalk in plant disease resistance. Plant Sci. 207:79-87. https://doi.org/10.1016/j.plantsci.2013.03.004
  25. Dermastia, M., Bertaccini, A., Constable, F. and Mehle, N. 2017. Grapevine yellows diseases and their phytoplasma agents: biology and detection. Springer, Cham, Netherlands. 99 pp.
  26. Dikilitas, M., Simsek, E. and Roychoudhur, A. 2020. Role of proline and glycine betaine in overcoming abiotic stresses. In: Protective chemical agents in the amelioration of plant abiotic stress: biochemical and molecular perspectives, eds. by A. Roychoudhury and D. K. Tripathi, pp. 1-23. John Wiley and Sons, Hoboken, NJ, USA.
  27. Duduk, B., Paltrinieri, S., Lee, I.-M. and Bertaccini, A. 2013. Nested PCR and RFLP analysis based on the 16S rRNA gene. Methods Mol. Biol. 938:159-171. https://doi.org/10.1007/978-1-62703-089-2_14
  28. Gawel, E. and Grzelak, M. 2014. Protein from lucerne in animals supplement diet. J. Food Agric. Environ. 12:314-319.
  29. Ghoulam, C., Foursy, A. and Fares, K. 2002. Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ. Exp. Bot. 47:39-50. https://doi.org/10.1016/S0098-8472(01)00109-5
  30. Guldur, M. E., Simsek, E., Gumus, H., Ayvaci, H. and Korkmaz, G. 2019. Garft transmibility of Canditatus Phytoplasma solani to pistachio rootstocks. In: Turkey VII Plant Protection Congress, Mugla, Turkey.
  31. Hameed, S., Akhtar, K. P., Hameed, A., Gulzar, T., Kiran. S., Yousaf, S., Abbas, G., Asghar, M. J. and Sarwar, N. 2017. Biochemical changes in the leaves of mungbean (Vigna radiata) plants infected by phytoplasma. Turk. J. Biochem. 42:591-599. https://doi.org/10.1515/tjb-2016-0304
  32. He, M., He, C.-Q. and Ding, N.-Z. 2018. Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Front. Plant Sci. 9:1771. https://doi.org/10.3389/fpls.2018.01771
  33. Heath, R. L. and Packer, L. 1968. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125:189-198. https://doi.org/10.1016/0003-9861(68)90654-1
  34. Hong, Y., Zhao, J., Guo, L., Kim, S.-C., Deng, X., Wang, G., Zhang, G., Li, M. and Wang, X. 2016. Plant phospholipases D and C and their diverse functions in stress responses. Prog. Lipid Res. 62:55-74. https://doi.org/10.1016/j.plipres.2016.01.002
  35. Jayaraj, J., Bhuvaneswari, R., Rabindran, R., Muthukrishnan, S. and Velazhahan, R. 2010. Oxalic acid-induced resistance to Rhizoctonia solani in rice is associated with induction of phenolics, peroxidase and pathogenesis-related proteins. J. Plant Interact. 5:147-157. https://doi.org/10.1080/17429140903291012
  36. Janmohammadi, M., Zolla, L. and Rinalducci, S. 2015. Low temperature tolerance in plants: changes at the protein level. Phytochemistry 117:76-89. https://doi.org/10.1016/j.phytochem.2015.06.003
  37. Junqueira, A., Bedendo, I. and Pascholati, S. 2004. Biochemical changes in corn plants infected by the maize bushy stunt phytoplasma. Physiol. Mol. Plant Pathol. 65:181-185. https://doi.org/10.1016/j.pmpp.2005.01.005
  38. Karakas, S. D. 2013. Development of tomato growing in soils differing in salt levels and effects of companion plants on some physiological parameters and soil remediation. Ph.D. thesis. Harran University, Sanliurfa, Turkey.
  39. Karakas, S., Dikilitas, M. and Akkurak, H. 2021. Biochemical and DNA damage responses of hydroponically grown Elands sourfig (Carpobrotus acinaciformis L.) leaves to cadmium stress conditions. Appl. Ecol. Environ. Res. 19:2649-2666. https://doi.org/10.15666/aeer/1904_26492666
  40. Karakas, S., Dikilitas, M., Almaca, A. and Tipirdamaz, R. 2020. Physiological and biochemical responses of (Aptenia cordifolia) to salt stress and its remediative effect on saline soils. Appl. Ecol. Environ. Res. 18:1329-1345. https://doi.org/10.15666/aeer/1801_13291345
  41. Karakas, S., Dikilitas, M. and Tipirdamaz, R. 2019. Biochemical and molecular tolerance of Carpobrotus acinaciformis L. halophyte plants exposed to high level of NaCl stress. Harran J. Agric. Food Sci. 23:99-107.
  42. Kim, Y.-N., Khan, M. A., Kang, S.-M., Hamayun, M. and Lee, I.-J. 2020. Enhancement of drought-stress tolerance of Brassica oleracea var. italica L. by newly isolated Variovorax sp. YNA59. J. Microbiol. Biotechnol. 30:1500-1509. https://doi.org/10.4014/jmb.2006.06010
  43. Kubalt, K. 2016. The role of phenolic compounds in plant resistance. Biotechnol. Food Sci. 80:97-108.
  44. Lopes, M., Sanches-Silva, A., Castilho, M., Cavaleiro, C. and Ramos, F. 2021. Halophytes as source of bioactive phenolic compounds and their potential applications. Crit. Rev. Food Sci. Nutr. Advanced online publication. https://doi.org/10.1080/10408398.2021.1959295.
  45. Magbanua, Z. V., De Moraes, C. M., Brooks, T. D., Williams, W. P. and Luthe, D. S. 2007. Is catalase activity one of the factors associated with maize resistance to Aspergillus flavus? Mol. Plant-Microbe Interact. 20:697-706. https://doi.org/10.1094/MPMI-20-6-0697
  46. Manga, I., Acar, Z. and Ayan, I. 2003. Leguminous forage crops. Ondokuz Mayis University, Faculty of Agriculture, Samsun, Turkey. 7 pp.
  47. Matilla-Vazquez, M. A. and Matilla, A. J. 2014. Ethylene: role in plants under environmental stress. In: Physiological mechanisms and adaptation strategies in plants under changing environment, eds. by P. Ahmad and M. R. Wani, Vol. 2, pp. 189-222. Springer, New York, USA.
  48. Milosevic, N. and Slusarenko, A. J. 1996. Active oxygen metabolism and lignification in the hypersensitive response in bean. Physiol. Mol. Plant Pathol. 49:143-158. https://doi.org/10.1006/pmpp.1996.0045
  49. Minitab Inc. 2020. Minitab 20 Statistical Software. Minitab Inc., State College, PA, USA.
  50. Naliwayski, M. and Sklodowska, M. 2021. The relationship between the antioxidant system and proline metabolism in the leaves of cucumber plants acclimated to salt stress. Cells 10:609. https://doi.org/10.3390/cells10030609
  51. Negro, C., Sabella, E., Nicoli, F., Pierro, R., Materazzi, A., Panattoni, A., Apriel, A., Nutricati, E., Vergine, M., Miceli, A., De Bellis, L. and Luvisi, A. 2020. Biochemical changes in leaves of Vitis vinifera cv. Sangiovese infected by bois noir phytoplasma. Pathogens 9:269. https://doi.org/10.3390/pathogens9040269
  52. Niu, Y. and Xiang, Y. 2018. An overview of biomembrane functions in plant responses to high-temperature stress. Front. Plant Sci. 9:915. https://doi.org/10.3389/fpls.2018.00915
  53. Ozyazici, M. A., Dengiz, O. and Saglam, M. 2013. Evaluation of potential nutritional problems and fertility status of the alfalfa (Medicago sativa L.) grown soils of artvin province. Artvin Coruh Univ. J. For. Fac. 14:225-238.
  54. Pan, R., Liu, J., Wang, S. and Hu, J. 2020. Peroxisomes: versatile organelles with diverse roles in plants. New Phytol. 225:1410-1427. https://doi.org/10.1111/nph.16134
  55. Patel, S. J., Subramanian, R. B. and Jha, Y. S. 2011. Biochemical and molecular studies of early blight disease in tomato. Phytoparasitica 39:269-283. https://doi.org/10.1007/s12600-011-0156-6
  56. Pieterce, C. M. J., Van Der Does, D., Zamioudis, C., Leon-Reyes, A. and Van Wees, S. C. M. 2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489-521. https://doi.org/10.1146/annurev-cellbio-092910-154055
  57. Poor, P., Borbely, P., Bodi, N., Bagyanszki, M. and Tari, I. 2019. Effects of salicylic acid on photosynthetic activity and chloroplast morphology under light and prolonged darkness. Photosynthetica 57:367-376. https://doi.org/10.32615/ps.2019.040
  58. Raiesi, T. and Golmohammadi, M. 2020. Changes in nutrient concentrations and biochemical characteristics of Mexican lime (Citrus aurantifolia) infected by phytoplasma. J. Gen. Plant Pathol. 86:486-493. https://doi.org/10.1007/s10327-020-00944-0
  59. Rainsford, K. D. 2004. Aspirin and related drugs. Taylor & Francis, London, UK, pp. 1-23.
  60. Rasouli, H., Farzaei, M. H., Mansouri, K., Mohammadzadeh, S. and Khodarahmi, R. 2016. Plant cell cancer: may natural phenolic compounds prevent onset and development of plant cell malignancy? A literature review. Molecules 21:1104. https://doi.org/10.3390/molecules21091104
  61. Rawat, N., Singla-Pareek, S. L. and Pareek, A. 2020. Membrane dynamics during individual and combined abiotic stresses in plants and tools to study the same. Physiol. Plant. 171:653-676.
  62. Raza, A., Charagh, S., Zahid, Z., Mubarik, M. S., Javed, R., Siddiqui, M. H. and Hasanuzzaman, M. 2021. Jasmonic acid: a key frontier in conferring abiotic stress tolerance in plants. Plant Cell Rep. 40:1513-1541. https://doi.org/10.1007/s00299-020-02614-z
  63. Rosahl, S. and Feussner, I. 2004. Oxylipins. In: Plant lipids: biology, utilisation and manipulation, ed. by D. J. Murphy, pp. 329-454. Blackwell, Oxford, UK.
  64. Salari, M., Panjehkeh, N., Nasirpoor, Z. and Abkhoo, J. 2012. Reaction of melon (Cucumis melo L.) cultivars to soil-borne plant pathogenic fungi in Iran. Afr. J. Biotechnol. 11:15324-15329.
  65. Sharma, P. and Gayen, D. 2021. Plant protease as regulator and signaling molecule for enhancing environmental stress-tolerance. Plant Cell Rep. 40:2081-2095. https://doi.org/10.1007/s00299-021-02739-9
  66. Shetty, K., Curtis, O. F., Levin, R. E., Wikowsky, R. and Ang, W. 1995. Prevention of verification associated with in vitro shoot culture of oregano (Origanum vulgare) by Pseudomonas spp. J. Plant Physiol. 147:447-451. https://doi.org/10.1016/S0176-1617(11)82181-4
  67. Siddique, Z., Akhtar, K. P., Hameed, A., Sarwar, N., Haq, I. U. and Khan, S. A. 2014. Biochemical alterations in leaves of resistant and susceptible cotton genotypes infected systemically by cotton leaf curl Burewala virus. J. Plant Interact. 9:702-711. https://doi.org/10.1080/17429145.2014.905800
  68. Singh, H. P., Kaur, S., Batish, D. R. and Kohli, R. K. 2014. Ferulic acid impair rhizogenesis and root growth, and alters associated biochemical changes in mung bean (Vigna radiata) hypocotyls. J. Plant Interact. 9:267-274. https://doi.org/10.1080/17429145.2013.820360
  69. Staswick, P. E. 1994. Storage proteins of vegetative plant tissues. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:303-322. https://doi.org/10.1146/annurev.pp.45.060194.001511
  70. Sugio, A., MacLean, A. M., Kingdom, H. N., Grieve, V. M., Manimekalai, R. and Hogenhout, S. A. 2011. Diverse targets of phytoplasma effectors: from plant development to defense against insects. Annu. Rev. Phytopathol. 49:175-195. https://doi.org/10.1146/annurev-phyto-072910-095323
  71. Tuladhar, P., Sasidharan, S. and Saudagar, P. 2021. Role of phenols and polyphenols in plant defense response to biotic and abiotic stresses. In: Biocontrol agents and secondary metabolites: applications and immunization for plant growh and protection, ed. by S. Jogaiah, pp. 419-441. Woodhead Publishing, Cambridge, UK.
  72. Turan, N., Celen, A. E. and Ozyazici, M. A. 2017. Yield and quality characteristics of some alfalfa (Medicago sativa L.) varieties grown in the Eastern Turkey. Turk. J. Field Crops 22:160-165.
  73. Wang, X.-S. and Han, J.-G. 2009. Changes of proline content, activity, and active isoforms of antioxidative enzymes in two alfalfa cultivars under salt stress. Agric. Sci. Chin. 8:431-440. https://doi.org/10.1016/S1671-2927(08)60229-1
  74. Warrier, R. R., Paul, M. and Vineetha, M. V. 2013. Estimation of salicylic acid in Eucalyptus leaves using spectrophotometric methods. Genet. Plant Physiol. 3:90-97.
  75. Xue, C., Liu, Z., Dai, L., Bu, J., Liu, M., Zhao, Z., Jiang, Z., Gao, W. and Zhao J. 2018. Changing host photosynthetic, carbohydrate, and energy metabolisms play important roles in phytoplasma infection. Phytopathology 108:1067-1077. https://doi.org/10.1094/phyto-02-18-0058-r
  76. Yang, R. R., Han, Y., Han, Z., Ackah, S., Li, Z., Bi, Y., Yang, Q. and Prusky, D. 2020. Hot water dipping stimulated wound healing of potato tubers. Postharvest Biol. Technol. 167:111245. https://doi.org/10.1016/j.postharvbio.2020.111245
  77. Yasmin, H., Bano, A., Wilson, N. L., Nosheen, A., Naz, R., Hassan, M. N., Ilyas, N., Saleem, M. H., Noureldeen, A., Ahmad, P. and Kennedy, I. 2021. Drought-tolerant Pseudomonas sp. showed differential expression of stress-responsive genes and induced drought tolerance in Arabidopsis thaliana. Physiol. Plant. 174:e13497.
  78. Zafari, S., Niknam, V., Musetti, R. and Noorbakhsh, S. N. 2012. Effect of phytoplasma infection on metabolite content and antioxidant enzyme activity in lime (Citrus aurantifolia). Acta Physiol. Plant. 34:561-568. https://doi.org/10.1007/s11738-011-0855-0