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Research Article

Arbuscular mycorrhizal fungi mitigate drought stress in citrus by modulating root microenvironment

, , ORCID Icon, ORCID Icon & ORCID Icon
Pages 1217-1228 | Received 10 Jul 2020, Accepted 17 Jan 2021, Published online: 25 Jan 2021

References

  • Ahmad S, Veyrat N, Gordon-Weeks R, Zhang Y, Martin J, Smart L, Glauser G, Erb M, Flors V, Frey M, et al. 2011. Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol. 157:317‒327.
  • Al-Abd NM, Nor ZM, Mansor M, Azhar F, Hasan MS, Kassim M. 2015. Antioxidant, antibacterial activity, and phytochemical characterization of Melaleuca cajuputi extract. BMC Complem Altern M. 15:385.
  • Augé RM, Stodola AJW, Tims JE, Saxton AM. 2001. Moisture retention properties of a mycorrhizal soil. Plant Soil. 230:87‒97.
  • Azaizeh HA, Marschner HR, Mheld V, Wittenmayer L. 1995. Effects of a vesicular-arbuscular mycorrhizal fungus and other soil microorganisms on growth, mineral nutrient acquisition and root exudation of soil-grown maize plants. Mycorrhiza. 5:321‒327.
  • Badri DV, Weir TL, Lelie DV, Vivanco JM. 2009. Rhizosphere chemical dialogues: plant microbe interactions. Curr Opin Biotechnol. 20:642‒650.
  • Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248‒252.
  • Clarkson DT, Marschner H. 1995. Mineral nutrition of higher plants. London: Academic Press.
  • Ding X, Fu L, Liu C, Chen F, Hoffland E, She J, Zhang F, Feng G. 2011. Positive feedback between acidification and organic phosphate mineralization in the rhizosphere of maize (Zea mays L.). Plant Soil. 349:13‒24.
  • Doornbos RF, Loon LCV, Bakker PAHM. 2012. Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev. 32:227‒243.
  • Elias KS, Safir GR. 1987. Hyphal elongation of Glomus fasciculatus in response to root exudates. Appl Environ Microb. 53:1928‒1933.
  • Gao Y, Zhou Z, Ling W, Hu X, Chen S. 2017. Glomalin-related soil protein enhances the availability of polycyclic aromatic hydrocarbons in soil. Soil Biol Biochem. 107:129‒132.
  • Graham JH. 1982. Effect of citrus root exudates on germination of chlamydosporas of the vesicular-arbuscular mycorrhizal fungus, Glomus epigaeum. Mycologia. 74:831‒835.
  • Harsh PB, Tiffany LW, Laura GP, Simon G, Jorge MV. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol. 57:233‒266.
  • Hashem A, Kumar A, Al-Dbass AM, Alqarawi AA, Al-Arjani AF, Singh G, Farooq M, Abd_Allah EF. 2019. Arbuscular mycorrhizal fungi and biochar improves drought tolerance in chickpea. Saudi J Biol Sci. 26:614‒624.
  • He JD, Chi GG, Zou YN, Shu B, Wu QS, Srivastava AK, Kuča K. 2020a. Contribution of glomalin-related soil proteins to soil organic carbon in trifoliate orange. Appl Soil Ecol. 154:103592.
  • He JD, Dong T, Wu HH, Zou YN, Wu QS, Kuča K. 2019. Mycorrhizas induce diverse responses of root TIP aquaporin gene expression to drought stress in trifoliate orange. Sci Hortic. 243:64–69.
  • He JD, Zou YN, Wu QS, Kuča K. 2020b. Mycorrhizas enhance drought tolerance of trifoliate orange by enhancing activities and gene expression of antioxidant enzymes. Sci Hortic. 262:108745.
  • Jones DL, Nguyen C, Finlay RD. 2009. Carbon flow in the rhizosphere: carbon trading at the soil root interface. Plant Soil. 321: 5‒33
  • Kemper WD, Rosenau R. 1986. Aggregate stability and size distribution. In: Klute A, editor. Methods of soil analysis, part 1. physical and mineralogical methods. Agronomy Monograph. American Society of Agronomy and Soil Science Society of America, Madison, USA; p. 425‒442.
  • Kiers ET, Heijden MG. 2006. Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology. 87:1627‒1636.
  • Koide RT, Kabir Z. 2000. Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol. 148:511‒517.
  • Korzekwa K. 2019. New proximal sensing approach to measure soil aggregate stability. CAS News. 64:4‒5.
  • Lǚ LH, Zou YN, Wu QS. 2019. Mycorrhizas mitigate soil replant disease of peach through regulating root exudates, soil microbial population, and soil aggregate stability. Commun Soil Sci Plant Anal. 50:909‒921.
  • Li G, Bai WB, Ren AX. 2017. Effects of continuous cropping duration of sorghum on components of root exudates and contents of allelochemicals. Chin J Ecol. 36:3535‒3544.
  • Mclachlan KD, Elliot DE, De Marco DG, Garran JH. 1987. Leaf acid phosphatase isozymes in the diagnosis of phosphorus status in field-grown wheat. Aust J Agric Res. 38:1‒13.
  • Nichols KA. 2008. Indirect contributions of AM fungi and soil aggregation to plant growth and protection. In: Siddiqui ZA, Akhtar MS, Futai K, editors. Mycorrhizae: sustainable Agriculture and Forestry. Berlin: Springer; p. 177‒194.
  • Park WJ, Hochholdinger F, Gierl A. 2004. Release of the benzoxazinoids defense molecules during lateral- and crown root emergence in Zea mays. J Plant Physiol. 161:981‒985.
  • Phillips JM, Hayman DS. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc. 55:158‒161.
  • Richardson AE, Simpson RJ. 2011. Soil microorganisms mediating phosphorus availability. Plant Physiol. 156:989‒996.
  • Rillig MC. 2004. Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci. 84:355‒363.
  • Sato T, Hachiya S, Inamura N, Ezawa T, Cheng WG, Tawaraya K. 2019. Secretion of acid phosphatase from extraradical hyphae of the arbuscular mycorrhizal fungi Rhizophagus clarus is regulated in response to phosphate availability. Mycorrhiza. 29:599–605.
  • Schwab SM, Leonard RT, Menge JA. 1984. Quantitative and qualitative comparison of root exudates of mycorrhizal and nonmycorrhizal plant species. Can J Bot. 62:1227–1231.
  • Susanne W, Roel W, Arjen B, Wim H, Putten VD. 2010. Microorganisms and nematodes increase levels of secondary metabolites in roots and root exudates of Plantago lanceolata. Plant Soil. 329:117‒126.
  • Tawaraya K, Watanabe S, Yoshida E, Wagatsuma T. 1995. Effect of onion (Allium cepa) root exudates on the hyphal growth ofgigaspora margarita. Mycorrhiza. 6:57‒59.
  • Vuković R, Bauer N, ĆurkovićPerica M. 2013. Genetic elicitation by inducible expression of β-cryptogein stimulates secretion of phenolics from Coleus blumei hairy roots. Plant Sci. 199-200:18‒28.
  • Wright SF, Franke-Snyder M, Morton JB, Upadhyaya A. 1996. Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant Soil. 181:193‒203.
  • Wu QS, He JD, Srivastava AK, Zou YN, Kuča K. 2019. Mycorrhizas enhance drought tolerance of citrus by altering root fatty acid compositions and their saturation levels. Tree Physiol. 39(7):1149–1158.
  • Wu QS, Li Y, Zou YN, He XH. 2015a. Arbuscular mycorrhiza mediates glomalin-related soil protein production and soil enzyme activities in the rhizosphere of trifoliate orange grown under different P levels. Mycorrhiza. 25:121‒130.
  • Wu QS, Srivastava AK, Li Y. 2015b. Effects of mycorrhizal symbiosis on growth behavior and carbohydrate metabolism of trifoliate orange under different substrate P levels. J Plant Growth Regul. 34:499‒508.
  • Wu QS, Srivastava AK, Zou YN. 2013. AMF-induced tolerance to drought stress in citrus: A review. Sci Hortic. 164:77‒87.
  • Wu QS, Wang YS, Xia RX. 2006. Comparision of arbuscular mycorrhizal fungi for drought resistance of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Acta Hortic Sin. 33:613‒616.
  • Xiao L, Liu GB, Li P, Xue J. 2017. Effects of short-term elevated CO2 concentration and drought stress on the rhizosphere effects of soil carbon, nitrogen and microbes of Bothriochloa ischaemum. Chin J Appl Ecol. 28:3251‒3259.
  • Yao Q, Li XL, Feng G. 2001. Mobilization of sparingly soluble inorganic phosphates by external mycelium of an arbuscular mycorrhizal fungus. Plant Soil. 230:279‒285.
  • Yu J, Wang LM, Walzem RL, Miller EG, Pike LM, Patil BS. 2005. Antioxidant activity of citrus limonoids, flavonoids, and coumarins. J Agric Food Chem. 53:2009‒2014.
  • Zhang F, Zou YN, Wu QS. 2018. Quantitative estimation of water uptake by mycorrhizal extraradical hyphae in citrus under drought stress. Sci Hortic. 229:132‒136.
  • Zhang F, Zou YN, Wu QS, Kuča K. 2020. Arbuscular mycorrhizas modulate root polyamine metabolism to enhance drought tolerance of trifoliate orange. Environ Exp Bot. 171:103962.
  • Zou YN, Srivastava AK, Wu QS. 2016. Glomalin: a potential soil conditioner for perennial fruits. Int J Agric Biol. 18:293‒297.
  • Zou YN, Srivastava AK, Wu QS, Huang YM. 2014. Glomalin-related soil protein and water relations in mycorrhizal citrus (Citrus tangerina) during soil water deficit. Arch Agron Soil Sci. 60:1103‒1114.
  • Zou YN, Wu HH, Giri B, Wu QS, Kuča K. 2019. Mycorrhizal symbiosis down-regulates or does not change root aquaporin expression in trifoliate orange under drought stress. Plant Physiol Biochem. 144:292‒299.
  • Zou YN, Wu QS, Kuča K. 2020. Unravelling the role of arbuscular mycorrhizal fungi in mitigating the oxidative burst of plants under drought stress. Plant Biol. doi:https://doi.org/10.1111/plb.13161.

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