Mycorrhiza Regulates Signal Substance Levels and Pathogen Defense Gene Expression to Resist Citrus Canker

Authors

  • Miao-Miao XIE Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Yi-Can ZHANG Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Li-Ping LIU Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Ying-Ning ZOU Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025 (CN)
  • Qiang-Sheng WU Yangtze University, College of Horticulture and Gardening, Jingzhou, Hubei 434025; University of Hradec Kralove, Faculty of Science, Department of Chemistry, Hradec Kralove 50003 (CN) https://orcid.org/0000-0002-3405-8409
  • Kamil KUČA University of Hradec Kralove, Faculty of Science, Department of Chemistry, Hradec Kralove 50003 (CZ) https://orcid.org/0000-0001-9664-1109

DOI:

https://doi.org/10.15835/nbha47411561

Keywords:

arbuscular mycorrhizal fungi; canker; pathogenesis related gene; salicylic acid

Abstract

Citrus canker is a quarantined disease, severely harming citrus plants. Soil beneficial arbuscular mycorrhizal fungi (AMF) can provide a biological control pathway to resist pathogens. This work was to test changes of signal substances including hydrogen peroxide (H2O2), nitric oxide (NO), calmodulin (CaM), salicylic acid (SA) and jasmonic acid (JA) and the pathogen defense gene expression in roots of AMF (Paraglomus occultum) and non-AMF trifoliate orange (Poncirus trifoliata) seedlings after infected by a expressions citrus canker pathogen (Xanthomonas axonopodis pv. Citri, Xac). AMF inoculation significantly improved plant height, stem diameter and leaf number. Xac infection dramatically decreased root H2O2, NO, and SA levels, but increased root CaM and JA concentrations in non-AMF seedlings. There were higher H2O2 and CaM levels and lower JA levels in Xac-infected seedlings than in non-Xac-infected seedlings under mycorrhization. Under non-Xac infection, mycorrhizal treatment reduced root H2O2, NO, and SA but increased CaM and JA levels. However, under Xac infection, mycorrhizal inoculation distinctly accelerated root H2O2, NO, CaM, and SA accumulation, accompanied with up-regulated expression levels of root PtEPS1 (enhance pseudomonas susceptibility 1) and PtPR4 (pathogenesis related gene 4), indicating that Xac stimulated mycorrhizal roles in enhancing resistance of citrus canker. Such results imply that citrus plants with pre-inoculated AMF had stronger resistance to Xac infection through increasing signal substrate accumulation and pathogen defense gene expressions.

References

Amir H, Cavaloc Y, Laurent A (2019). Arbuscular mycorrhizal fungi and sewage sludge enhance growth and adaptation of Metrosideros laurifolia on ultramafic soil in New Caledonia: A field experiment. Science of the Total Environment 651(1):334-343.

Azami-Sardooei Z, Franca SC, De Vlesschauwer D, Höfte M (2010). Riboflavin induces resistance against Botrytis cinerea in bean, but not in tomato, by priming for a hydrogen peroxide-fueled resistance response. Physiological and Molecular Plant Pathology 75(1-2):23-29.

Bethlenfalvay GJ, Ames RN (1987). Comparison of two methods for quantifying extraradical mycelium of vesicular arbuscular mycorrhizal fungi. Soil Science Society of America Journal 51(3):834-837.

Chandrasekhar B, Umesha S, Naveen Kumar HN (2017). Proteominc analysis of salicylic acid enhanced disease resistance in bacterial wilt affected chili (Capsicum annuum) crop. Physiological and Molecular Plant Pathology 98:85-96.

Das AK (2003). Citrus canker - A review. Journal of Applied Horticulture 5(1):52-60.

DeFalco TA, Bender KW, Snedden WA (2010). Breaking the code: Ca2+ sensors in plant signaling. Biochemical Journal 425(1):27-40.

Delledonne M (2005). NO news is good news for plant. Current Opinion in Plant Biology 8(4):390-396.

Deng ZN, Xu L, Long GY, Liu LP, Fang FF, Shu GP (2010). Screening citrus genotypes for resistance to canker disease (Xanthomonas axonopodis pv. citri). Plant Breeding 129(3):341-345.

Foissner I, Wendehenne D, Langebartels C, Durner J (2000). In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant Journal 23(6):817-824.

Gallou A, Mosquera HPL, Cranenbrouck S, Suárez JP, Declerck S (2017). Mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans. Physiological and Molecular Plant Pathology 76(1):20-26.

Ghorchiani M, Etesami H, Alikhani HA (2018). Improvement of growth and yield of maize under water stress by co-inoculating an arbuscular mycorrhizal fungus and a plant growth promoting rhizobacterium together with phosphate fertilizers. Agriculture Ecosystems and Environment 258:59-70.

Grant, JJ, Loake, GJ (2000). Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiology 124(1):21-29.

Huang YM, Srivastava AK, Zou YN, Ni QD, Han Y, Wu QS (2014). Mycorrhizal-induced calmodulin mediated changes in antioxidant enzymes and growth response of drought-stressed trifoliate orange. Frontiers in Microbiology 5(682):1-7.

Kim MC, Chung WS, Yun DJ, Cho MJ (2009). Calcium and calmodulin-mediated regulation of gene expression in plants. Molecular Plant 2(1):13-21.

Lamb C, Dixon RA (1997). The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48(1):251-275.

Lindermayr J, Saalbach G, Durner J (2005). Proteomic identification of S-nitrisylated proteins in Arabidopsis. Plant Physiology 137(3):921-930.

Liu JY, Maldonado-Mendoza L, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007). Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant Journal 50(3):529-544.

Liu LP, Deng ZN, Qu JW, Yan JW, Catara V, Li DZ, Long GY, Li N (2012). Construction of EGFP-labeling system for visualizing the infection process of Xanthomonas axonopodis pv. citriinplanta. Current Microbiology 65(3):304-312.

Livak LJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and 2−ΔΔCt method. Methods 25(4):402-408.

Lorella N, Moscatiello R, Genre A, Novero M, Bonfante P, Mariani P (2007). The arbuscular mycorrhizal fungus Glomus intraradices induces intracellular calcium changes in soybean cells. Caryologia 60(1-2):137-140.

Maya MA, Matsubara YI (2013). Tolerance to Fusarium wilt and anthracnose diseases and changes of antioxidative activity in mycorrhizal cyclamen. Crop Protection 47(5):41-48.

Mohase L, der Westhuizen AJ, Pretorius ZA (2011). Involvement of reactive oxygen species generating enzymes and hydrogen peroxide in the rust resistance response of sunflower (Helianthus annuus L.). South African Journal of Plant and Soil 28(1):64-68.

Nair A, Kolet SP, Thilasiram HV, Bhargava S (2015). Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternate. Plant Biology 17(3):625-631.

Nair A, Kolet SP, Thulasiram HV, Bhargava S (2105). Role of methyl jasmonate in the expression of mycorrhizal induced resistance against Fusarium oxysporum in tomato plants. Physiological and Molecular Plant Pathology 92:139-145.

Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002). Hydrogen peroxide and nitric oxide as signalling molecules in plants. Journal of Experimental Botany 53(372):1237-1247.

Oyewole BO, Olawuyi OJ, Odebode AC, Abiala MA (2017). Influence of arbuscular mycorrhiza fungi (AMF) on drought tolerance and charcoal rot disease of cowpea. Biotechnology Reports 14:8-15.

Parniske M (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6(10):763-775.

Phillips JM, Hayman DS (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55(1):158-161.

Romero-Puertas MC, Perazzolli M, Zago E, Delledonne M (2004). Nitric oxide signaling functions in plant interaction. Cellular Microbiology 6(9):795-803.

Shao YD, Zhang DJ, Hu XC, Wu QS, Jiang CJ, Xia TJ, Gao XB, Kuča K (2018). Mycorrhiza-induced changes in root growth and nutrient absorption of tea plants. Plant Soil and Environment 64(6):283-289.

Sharma IP, Sharma AK (2017). Co-inoculation of tomato with an arbuscular mycorrhizal fungus improves plant immunity and reduces root-knot nematode. Rhizosphere 4:25-28.

Song YY, Chen DM, Lu K, Sun ZX, Zeng R (2015). Enhances tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science 6(786):1-13.

Spoel SH, Dong X (2008). Making sense of hormone crosstalk during plant immune response. Cell Host Microbe 3(6):348-351.

Vani MS, Hindumathi A, Reddy BN (2018). Beneficial effect of arbuscular mycorrhizal fungus, Glomus fasciculatum, on plant growth and nutrient uptake in tomato. Indian Phytopathology 71(1):115-122.

Velikova V, Yordanov I, Edreva A (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protection of exogenous polyamines. Plant Science 15(1):59-66.

Wu G, Shortt BJ, Lawrence EB, Leo J, Fitzsimmons KC, Levine EB, Raskin I, Shah DM (1997). Activation of host defense mechanisms by elevated production of H2O2 in transgenic plants. Plant Physiology 115(2):427-435.

Wu QS, He JD, Srivastava AK, Zou YN, Kuca K (2019). Mycorrhizas enhance drought tolerance of citrus by altering root fatty acid compositions and their saturation levels. Tree Physiology 39(7):1149-1158.

Wu QS, Sun P, Srivastava AK (2017). AMF diversity in citrus rhizosphere. Indian Journal of Agricultural Sciences 87(5):653-656.

Zhang RQ, Zhu HH, Zhao HQ, Yao Q (2013). Arbuscular mycorrhizal fungal inoculation increases phenolic synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide signaling pathways. Journal of Plant Physiology 170(1):74-79.

Zhang Y, Xu S, Ding P, Wang DM, Cheng YT, He J, … Zhang YL (2010). Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proceedings of the National Academy of Sciences 107(42):18220-18225.

Zhang YC, Liu CY, Wu QS (2017a). Mycorrhizal and common mycorrhizal network regulated the production of signal substances in trifoliate orange (Poncirus trifoliata). Notulae Botanicae Horti Agrobotanici Cluj-Napoca 45(1):43-49.

Zhang YC, Liu LP, Zou YN, Liu CY, Wu QS (2017b). Response of signal substances to canker in trifoliate orange roots through mycorrhizal hyphal bridge. Mycosystema 36(7):1028-1036 (in Chinese with an English abstract).

Zhang YC, Zou YN, Liu LP, Wu QS (2019). Common mycorrhizal networks activated salicylic acid defense response of trifoliate orange (Poncirus trifoliata). Journal of Integrative Plant Biology 61(10):1099-1111.

Zou YN, Huang YM, Wu QS, He XH (2015). Mycorrhiza-induced lower oxidative burst is related with higher antioxidant enzyme activities, net H2O2 effluxes, and Ca2+ influxes in trifoliate orange roots under drought stress. Mycorrhiza 25(2):143-152.

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Published

2019-11-22

How to Cite

XIE, M.-M., ZHANG, Y.-C., LIU, L.-P., ZOU, Y.-N., WU, Q.-S., & KUČA, K. (2019). Mycorrhiza Regulates Signal Substance Levels and Pathogen Defense Gene Expression to Resist Citrus Canker. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 47(4), 1161–1167. https://doi.org/10.15835/nbha47411561

Issue

Vol. 47 No. 4 (2019)

Section

Research Articles
CITATION
DOI: 10.15835/nbha47411561

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Copyright (c) 2019 Miao-Miao XIE, Yi-Can ZHANG, Li-Ping LIU, Ying-Ning ZOU, Qiang-Sheng WU, Kamil KUČA

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