Silencing MdGH3-2/12 in apple reduces drought resistance by regulating AM colonization

Dong Huang , Qian Wang , Zhijun Zhang , Guangquan Jing , Mengnan Ma , Fengwang Ma , Chao Li

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 84

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :84 DOI: 10.1038/s41438-021-00524-z
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Silencing MdGH3-2/12 in apple reduces drought resistance by regulating AM colonization
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Abstract

Drought leads to reductions in plant growth and crop yields. Arbuscular mycorrhizal fungi (AMF), which form symbioses with the roots of the most important crop species, alleviate drought stress in plants. In the present work, we identified 14 GH3 genes in apple (Malus domestica) and provided evidence that MdGH3-2 and MdGH3-12 play important roles during AM symbiosis. The expression of both MdGH3-2 and MdGH3-12 was upregulated during mycorrhization, and the silencing of MdGH3-2/12 had a negative impact on AM colonization. MdGH3-2/12 silencing resulted in the downregulation of five genes involved in strigolactone synthesis, and there was a corresponding change in root strigolactone content. Furthermore, we observed lower root dry weights in RNAi lines under AM inoculation conditions. Mycorrhizal transgenic plants showed greater sensitivity to drought stress than WT, as indicated by their higher relative electrolytic leakage and lower relative water contents, osmotic adjustment ability, ROS scavenging ability, photosynthetic capacity, chlorophyll fluorescence values, and abscisic acid contents. Taken together, these data demonstrate that MdGH3-2/12 plays an important role in AM symbiosis and drought stress tolerance in apple.

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Dong Huang, Qian Wang, Zhijun Zhang, Guangquan Jing, Mengnan Ma, Fengwang Ma, Chao Li. Silencing MdGH3-2/12 in apple reduces drought resistance by regulating AM colonization. Horticulture Research, 2021, 8 (1) : 84 DOI:10.1038/s41438-021-00524-z

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References

[1]

Mendes, R., Garbeva, P. & Raaijmakers, J. M. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37, 634-663 (2013).

[2]

Bucher, M., Hause, B., Krajinski, F. & Kuster, H. Through the doors of perception to function in arbuscular mycorrhizal symbioses. N. Phytol. 204, 833-840 (2014).

[3]

Chitarra, W. et al. Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol. 171, 1009-1023 (2016).

[4]

Ruiz-Lozano, J. M. et al. Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ. 39, 441-452 (2016).

[5]

Remy, W., Taylor, T., Hass, H. & Kerp, H. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Nat. Acad. Sci. USA 91, 11841-11843 (1994).

[6]

Doidy, J. et al. The Medicago truncatula sucrose transporter family: characterization and implication of key members in carbon partitioning towards arbuscular mycorrhizal fungi. Mol. Plant 5, 1346-1358 (2012).

[7]

Baier, M. C. et al. Knockdown of the symbiotic sucrose synthase MtSucS1 affects arbuscule maturation and maintenance in mycorrhizal roots of Medicago truncatula. Plant Physiol. 152, 1000-1014 (2010).

[8]

Smith, S. E. & Smith, F. A. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant. Biol. 62, 227-250 (2011).

[9]

Guillotin, B. et al. Sl-IAA27 regulates strigolactone biosynthesis and mycorrhization in tomato (var. MicroTom). N. Phytol. 213, 1124-1132 (2017).

[10]

MacLean, A. M., Bravo, A. & Harrison, M. J. Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. Plant Cell 29, 2319-2335 (2017).

[11]

Akiyama, K., Matsuzaki, K. & Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824-827 (2005).

[12]

Charpentier, M., Sun, J., Wen, J., Mysore, K. S. & Oldroyd, G. E. Abscisic acid promotion of arbuscular mycorrhizal colonization requires a component of the PROTEIN PHOSPHATASE 2A complex. Plant Physiol. 166, 2077-2090 (2014).

[13]

Etemadi, M. et al. Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol. 166, 281-292 (2014).

[14]

Chory, J. et al. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLOS Biol. 4, e226 (2006).

[15]

Genre, A. et al. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone . N. Phytol. 198, 190-202 (2013).

[16]

Maillet, F. et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58-63 (2011).

[17]

Harrison, M. J. Cellular programs for arbuscular mycorrhizal symbiosis. Curr. Opin. Plant. Biol. 15, 691-698 (2012).

[18]

Martin, P. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763-775 (2008).

[19]

Foo, E., Ross, J. J., Jones, W. T. & Reid, J. B. Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann. Bot. 111, 769-779 (2013).

[20]

Herrera-Medina, M. J., Steinkellner, S., Vierheilig, H., Bote, J. A. O. & Garrido, J. M. G. Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. N. Phytol. 175, 554-564 (2007).

[21]

Santner, A., Calderon-Villalobos, L. I. & Estelle, M. Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5, 301-307 (2009).

[22]

Sun, X. et al. Overexpression of MdATG18a in apple improves resistance to Diplocarpon mali infection by enhancing antioxidant activity and salicylic acid levels. Hortic. Res. 5, 57 (2018a).

[23]

Jin, Y. et al. DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nat. Commun. 7, 12433 (2016).

[24]

Takeda, N. et al. Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus. Plant Physiol. 167, 545-557 (2015).

[25]

Hanlon, M. T. & Coenen, C. Genetic evidence for auxin involvement in arbuscular mycorrhiza initiation. N. Phytol. 189, 701-709 (2011).

[26]

Foo, E. Auxin influences strigolactones in pea mycorrhizal symbiosis. J. Plant Physiol. 170, 523-528 (2013).

[27]

Sheffield, J., Wood, E. F. & Roderick, M. L. Little change in global drought over the past 60 years. Nature 491, 435-438 (2012).

[28]

Trenberth, K. E. et al. Global warming and changes in drought. Nat. Clim. Chang. 4, 17-22 (2013).

[29]

Fan, Q. J. & Liu, J. H. Colonization with arbuscular mycorrhizal fungus affects growth, drought tolerance and expression of stress-responsive genes in Poncirus trifoliata. Acta Physiol. Plant 33, 1533-1542 (2011).

[30]

Mo, Y. L. et al. Regulation of plant growth, photosynthesis, antioxidation and osmosis by an arbuscular mycorrhizal fungus in watermelon seedlings under well-watered and drought conditions. Front. Plant Sci. 7, 644 (2016).

[31]

Wu, Q. S., He, J. D., Srivastava, A. K., Zou, Y. N. & Kuca, K. Mycorrhizas enhance drought tolerance of citrus by altering root fatty acid compositions and their saturation levels. Tree Physiol. 39, 1149-1158 (2019).

[32]

Farooq, M., Wahid, A., Kobayashi, N., Fujita, D. & Basra, S. M. A. Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29, 185-212 (2009).

[33]

Ruiz-Lozano, J. M. & Aroca, R. Modulation of aquaporin genes by the arbuscular mycorrhizal symbiosis in relation to osmotic stress tolerance. Symbioses Stress, Springe. Neth. 17, 359-374 (2010).

[34]

Osakabe, Y., Osakabe, K., Shinozaki, K. & Tran, L. S. Response of plants to water stress. Front. Plant Sci. 5, 86 (2014).

[35]

Talbi, S. et al. Drought tolerance in a saharian plant Oudneya africana: role of antioxidant defences. Environ. Exp. Bot. 111, 114-126 (2015).

[36]

Pierik, R. & Testerink, C. The art of being flexible: how to escape from shade, salt, and drought. Plant Physiol. 166, 5-22 (2014).

[37]

Miransari, M., Abrishamchi, A., Khoshbakht, K. & Niknam, V. Plant hormones as signals in arbuscular mycorrhizal symbiosis. Crit. Rev. Biotechnol. 34, 123-133 (2014).

[38]

Ruiz-Sanchez, M., Aroca, R., Munoz, Y., Polon, R. & Ruiz-Lozano, J. M. The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J. Plant Physiol. 167, 862-869 (2010).

[39]

Huang, D. et al. Arbuscular mycorrhizal fungi enhanced drought resistance in apple by regulating genes in the MAPK pathway. Plant Physiol. Biochem. 149, 245-255 (2020).

[40]

Liao, D. H. et al. The characterization of six auxin-induced tomato GH3 genes uncovers a member, SlGH3.4, strongly responsive to arbuscular mycorrhizal symbiosis. Plant Cell Physiol. 56, 674-687 (2015).

[41]

Campanella, J. J., Smith, S. M., Leibu, D., Wexler, S. & Ludwig-Müller, J. The auxin conjugate hydrolase family of Medicago truncatula and their expression during the interaction with two symbionts. J. Plant Growth Regul. 27, 26-38 (2008).

[42]

Abbaspour, H., Saeidi-Sar, S., Afshari, H. & Abdel-Wahhab, M. A. Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J. Plant Physiol. 169, 704-709 (2012).

[43]

Wang, S. C. et al. Influence of drought stress on the cellular ultrastructure and antioxidant system in leaves of drought-tolerant and drought-sensitive apple rootstocks. Plant Physiol. Biochem. 51, 81-89 (2012).

[44]

Sun, X. et al. Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple. Plant Biotechnol. J. 16, 545-557 (2018b).

[45]

Bahadur, A. et al. Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. Int. J. Mol. Sci. 20, 4199 (2019).

[46]

Dai, H. Y. et al. Development of a seedling clone with high regeneration capacity and susceptibility to Agrobacterium in apple. Sci. Horticulturae 164, 202-208 (2013).

[47]

Xie, Y. P. et al. An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple. N. Phytol. 218, 201-218 (2018).

[48]

Koske, R. E. & Gemma, J. N. A modified procedure for staining roots to detect VA mycorrhizas. Mycol. Res. 92, 486-505 (1989).

[49]

Trouvelot, A., Kough, J. L. & Gianinazzi-Pearson, V. Mesure du taux de mycorhization VA d’un systeme radiculaire. Recherche demethodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V., Gianinazzi S., eds Physiological and genetical aspects of mycorrhizae.INRA Press, Paris, France: Proceedings of the 1st European Symposium on mycorrhizae Institut National de la Recherche Agronomique, 217-221 (1986).

[50]

Batistic, O., Waadt, R., Steinhorst, L., Held, K. & Kudla, J. CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J. 61, 211-222 (2010).

[51]

Liu, Y. F. et al. Biochemical and functional characterization of AcUFGT3a, a galactosyltransferase involved in anthocyanin biosynthesis in the red-fleshed kiwifruit (Actinidia chinensis). Physiol. Plant. 162, 409-426 (2018).

[52]

Ma, Y. Q. et al. Induction of seed germination in Orobanche spp. by extracts of traditional Chinese medicinal herbs. Sci. China Life Sci. 55, 250-260 (2012).

[53]

Guo, T. L. et al. Overexpression of the RNA binding protein MhYTP1 in transgenic apple enhances drought tolerance and WUE by improving ABA level under drought condition. Plant Sci. 280, 397-407 (2019).

[54]

Dionisio-Sese, M. L. & Tobita, S. Antioxidant responses of rice seedlings to salinity stress. Plant Sci. 135, 1-9 (1998).

[55]

Huo, L. Q. et al. MdATG18a overexpression improves basal thermotolerance in transgenic apple by decreasing damage to chloroplasts. Hortic. Res. 7, 21 (2020).

[56]

Xu, D. B. et al. Identifcation and expression analysis of auxin-responsive GH3 family genes in Chinese hickory (Carya cathayensis) during grafting. Mol. Biol. Rep. 47, 4495-4506 (2020).

[57]

Yuan, H. Z. et al. Genome-wide analysis of the GH3 family in apple (Malus × domestica). BMC Genomics. 14, 297.

[58]

Jain, M., Kaur, N., Tyagi, A. K. & Khurana, J. P. The auxin-responsive GH3 gene family in rice (Oryza sativa). Funct. Integr. Genomic. 6, 36-46.

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