Ericoid mycorrhizal fungus enhances microcutting rooting of Rhododendron fortunei and subsequent growth

Xiangying Wei , Jianjun Chen , Chunying Zhang , Hong Liu , Xiuxia Zheng , Jingli Mu

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 140

PDF (1240KB)
Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :140 DOI: 10.1038/s41438-020-00361-6
Article
research-article
Ericoid mycorrhizal fungus enhances microcutting rooting of Rhododendron fortunei and subsequent growth
Author information +
History +
PDF (1240KB)

Abstract

Adventitious root (AR) formation is a unique feature of plant reproduction and plays a vital role in crop production as many horticultural and forestry plants are propagated through cuttings. A growing number of reports have shown that microbes, particularly mycorrhizal fungi are able to promote AR formation, but the underlying mechanisms remain largely unclear. This study established an in vitro culture system and investigated AR formation in microcuttings of Rhododendron fortunei Lindl. inoculated with Oidiodendron maius Barron Om19, an ericoid mycorrhizal fungus strain. Hormones and precursors involved in the biosynthesis of indole-3-acetic acid (IAA) in Om19 mycelium were analyzed. Om19 was able to produce a large quantity of tryptophan (Trp) and also indole-3-pyruvate (IPA) and IAA, indicating that IAA biosynthesis in Om19 could be through a Trp-dependent pathway. After inoculation of Om19, ARs were quickly formed in microcuttings. Symbiosis related genes were activated in ARs, and Om19 effectively colonized the roots. YUC3, a key gene in plant biosynthesis of IAA and genes involved in nitrogen (N) uptake and metabolism, phosphorus (P) uptake were highly upregulated. Plants absorbed significantly greater quantity of mineral nutrients, and their growth was substantially enhanced compared to the control plants without Om19 inoculation. A working model for Om19 enhanced AR formation was proposed. The rapid formation of ARs in cuttings could be due in part to the induction of IAA biosynthesized by Om19 and also attributed to Trp catalyzed biosynthesis of IAA in plants. AR formation, in turn, provided Om19 preferred sites for colonization. Our study suggested that in addition to promoting AR formation, Om19 could potentially be used as a new biofertilizer for enhancing production of ericaceous plants, such as blueberry, cranberry, and rhododendron.

Cite this article

Download citation ▾
Xiangying Wei, Jianjun Chen, Chunying Zhang, Hong Liu, Xiuxia Zheng, Jingli Mu. Ericoid mycorrhizal fungus enhances microcutting rooting of Rhododendron fortunei and subsequent growth. Horticulture Research, 2020, 7 (1) : 140 DOI:10.1038/s41438-020-00361-6

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Steffens, B. & Rasmussen, A. The physiology of adventitious roots. Plant Physiol. 170, 603-617 (2016).

[2]

Druege, U., Franken, P. & Hajirezaei, M. R. Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front. Plant Sci. 7, 381 (2016).

[3]

Chen, J. & Stamps, R. H. Cutting Propagation: A Guide To Propagating And Producing Floriculture Crops (eds. Dole J. M. & Gibson J. L.) Chapter 16 (Ball Publishing, Batavia, IL, 2006).

[4]

Druege, U. & Franken, P. Petunia as model for elucidating adventitious root formation and mycorrhizal symbiosis: at the nexus of physiology, genetics, microbiology and horticulture. Physiol. Plant. 165, 58-72 (2019).

[5]

Hartmann, H. T., Davies, J. F. T., Geneve, R. L. & Wilson, S. B. Hartmann and Kester’s Plant Propagation: Principles and Practices (Pearson Education, New York, NY, 2018).

[6]

Bellini, C., Pacurar, D. I. & Perrone, I. Adventitious roots and lateral roots: similarities and differences. Annu. Rev. Plant Biol. 65, 639-666 (2014).

[7]

Guan, L. et al. Physiological and molecular regulation of adventitious root formation. Crit. Rev. Plant Sci. 34, 506-521 (2015).

[8]

Fattorini, L. et al. Indole-3-butyric acid promotes adventitious rooting in Arabidopsis thaliana thin cell layers by conversion into indole-3-acetic acid and stimulation of anthranilate synthase activity. BMC Plant Biol. 17, 121 (2017).

[9]

Won, C. et al. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 18518-18523 (2011).

[10]

Yamada, M., Greenham, K., Prigge, M. J., Jensen, P. J. & Estelle, M. The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol. 151, 168-179 (2009).

[11]

Mashiguchi, K. et al. The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 18512-18517 (2011).

[12]

Cheng, Y., Dai, X. & Zhao, Y. Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19, 2430-2439 (2007).

[13]

Stepanova, A. N. et al. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133, 177-191 (2008).

[14]

Zhao, Y. et al. Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Gene. Dev. 16, 3100-3112 (2002).

[15]

Zhao, Y. et al. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291, 306-309 (2001).

[16]

Linderman, R. & Call, C. A. Enhanced rooting of woody plant cuttings by mycorrhizal fungi. J. Am. Soc. Hortic. Sci. 102, 629-632 (1977).

[17]

Sukumar, P. et al. Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions. Plant Cell Environ. 36, 909-919 (2013).

[18]

Vohník, M., Fendrych, M., Albrechtová, J. & Vosátka, M. Intracellular colonization of Rhododendron and Vaccinium roots by Cenococcum geophilum, Geomyces pannorum and Meliniomyces variabilis. Folia Microbiol. 52, 407-414 (2007).

[19]

Oliveira, P., Barriga, J., Cavaleiro, C., Peixe, A. & Potes, A. Z. Sustained in vitro root development obtained in Pinus pinea L. inoculated with ectomycorrhizal fungi. Forestry 76, 579-587 (2003).

[20]

Scagel, C., Reddy, K. & Armstrong, J . Mycorrhizal fungi in rooting substrate influences the quantity and quality of roots on stem cuttings of hick’s yew. HortTechnology 13, 62-66 (2003).

[21]

Scagel, C. F. Inoculation with ericoid mycorrhizal fungi alters fertilizer use of highbush blueberry cultivars. HortScience 40, 786-794 (2005).

[22]

Pandey, D., Kehri, H. K., Zoomi, I., Akhtar, O. & Singh, A. K. Recent Advancement in White Biotechnology through Fungi. Vol. 1: Deversity and Enzymes Perspectives (eds. Yadav, A. N., Mishra, S., Singh, S. & Gupta, A.) Chapter 5 (Springer Nature Switzeland AG, Cham, Switzerland, 2019).

[23]

Niemi, K. et al. Application of ectomycorrhizal fungi in rooting of Scots pine fascicular shoots. Can. J. Res. 30, 1221-1230 (2000).

[24]

Niemi, K., Scagel, C. & Haggman, H. Application of ectomycorrhizal fungi in vegetative propagation of conifers. Plant Cell Tissue Org. Cult. 78, 83-91 (2004).

[25]

Niemi, K., Vuorinen, T. & Ernstsen, A. Ectomycorrhizal fungi and exogenous auxins influence root and mycorrhiza formation of Scots pine hypocotyl cuttings in vitro. Tree Physiol. 22, 1231-1239 (2002).

[26]

Fehrer, J., Réblová, M., Bambasová, V. & Vohník, M. The root-symbiotic Rhizoscyphus ericae aggregate and Hyaloscypha (Leotiomycetes) are congeneric: Phylogenetic and experimental evidence. Stud. Mycol. 92, 195-225 (2019).

[27]

Kolařík, M. & Vohník, M. When the ribosomal DNA does not tell the truth: The case of the taxonomic position of Kurtia argillacea, an ericoid mycorrhizal fungus residing among Hymenochaetales. Fungal Biol. 122, 1-18 (2018).

[28]

Vohník, M., Pánek, M., Fehrer, J. & Selosse, M.-A. Experimental evidence of ericoid mycorrhizal potential within Serendipitaceae (Sebacinales). Mycorrhiza 26, 831-846 (2016).

[29]

Rice, A. V. & Currah, R. S. Microbial Root Endophytes (eds. Schulz, B. J. E., Boyle, C. J. C. & Sieber, T. N.) Chapter 13 (Springer, Heidelberg, Germany, 2006).

[30]

Wei, X., Chen, J., Zhang, C. & Wang, Z. In vitro shoot culture of Rhododendron fortunei: an important plant for bioactive phytochemicals. Ind. Crops Prod. 126, 459-465 (2018).

[31]

Gorecka, K. The effect of growth regulators on rooting of Ericaceae plants. Acta Hort. 91, 483-489 (1979).

[32]

Fan, S. et al. Micropropagation of blueberry ‘Bluejay’ and ‘Pink Lemonade’ through in vitro shoot culture. Sci. Hortic. 226, 277-284 (2017).

[33]

Qiu, D., Wei, X., Fan, S., Jian, D. & Chen, J. Regeneration of blueberry cultivars through indirect shoot organogenesis. HortScience 53, 1045-1049 (2018).

[34]

Scagel, C. F., Wagner, A. & Winiarski, P. Frequency and intensity of root colonization by ericoid mycorrhizal fungi in nursery production of blueberry plants. Small Fruits Rev. 4, 95-112 (2005).

[35]

Scagel, C. F., Wagner, A. & Winiarski, P. Inoculation with ericoid mycorrhizal fungi alters root colonization and growth in nursery production of blueberry plants from tissue culture and cuttings. Small Fruits Rev. 4, 113-135 (2005).

[36]

Wei, X., Chen, J., Zhang, C. & Pan, D. A new Oidiodendron maius strain isolated from Rhododendron fortunei and its effects on nitrogen uptake and plant growth. Front. Microbiol. 7, 1327 (2016).

[37]

Wei, X., Chen, J., Zhang, C. & Pan, D. Differential gene expression in Rhododendron fortunei roots colonized by an ericoid mycorrhizal fungus and increased nitrogen absorption and plant growth. Front. Plant Sci. 7, 1594 (2016).

[38]

Martino et al. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. N. Phytol. 217, 1213-1229 (2018).

[39]

Starrett, M. C., Blazich, F. A., Shafer, S. R. & Grand, L. F. In vitro colonization of micropropagated Pieris floribunda by ericoid mycorrhizae. II. Effects on acclimatization and growth. HortScience 36, 357-359 (2001).

[40]

Krause, K. et al. Biosynthesis and secretion of indole-3-acetic acid and its morphological effects on Tricholoma vaccinum-spruce ectomycorrhiza. Appl. Environ. Microbiol. 81, 7003-7011 (2015).

[41]

Felten et al. The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol. 151, 1991-2005 (2009).

[42]

Vayssieres, A. et al. Development of the poplar-Laccaria bicolor ectomycorrhiza modifies root auxin metabolism, signaling, and response. Plant Physiol. 169, 890-902 (2015).

[43]

Normand, L., Bärtschi, H., Debaud, J. C. & Gay, G. Rooting and acclimatization of micropropagated cuttings of Pinus pinaster and Pinus sylvestris are enhanced by the ectomycorrhizal fungus Hebeloma cylindrosporum. Physiol. Plant. 98, 759-766 (1996).

[44]

Gay, G., Normand, L., Marmeisse, R., Sotta, B. & Debaud, J. Auxin overproducer mutants of Hebeloma cylindrosporum Romagnesi have increased mycorrhizal activity. N. Phytol. 128, 645-657 (1994).

[45]

Rudawska, M. & Kieliszewska-Rokicka, B. Mycorrhizal formation by Paxillus involutus strains in relation to their IAA-synthesizing activity. N. Phytol. 137, 509-517 (1997).

[46]

Tranvan, H., Habricot, Y., Jeannette, E., Gay, G. & Sotta, B. Dynamics of symbiotic establishment between an IAA-overproducing mutant of the ectomycorrhizal fungus Hebeloma cylindrosporum and Pinus pinaster. Tree Physiol. 20, 123-129 (2000).

[47]

Liu, C.-Y. et al. Mycorrhiza stimulates root-hair growth and IAA synthesis and transport in trifoliate orange under drought stress. Sci. Rep. 8, 1978 (2018).

[48]

Wang, B. et al. Tryptophan-independent auxin biosynthesis contributes to early embryogenesis in Arabidopsis. Proc. Natl Acad. Sci. USA 112, 4821-4826 (2015).

[49]

Mano, Y. & Nemoto, K. The pathway of auxin biosynthesis in plants. J. Exp. Bot. 63, 2853-2872 (2012).

[50]

Kühn, C. et al. Brassinosteroids affect the symbiosis between the AM fungus Rhizoglomus irregularis and solanaceous host plants. Front. Plant Sci. 10, 571 (2019).

[51]

Felten, J., Legué, V. & Anicet Ditengou, F. Lateral root stimulation in the early interaction between Arabidopsis thaliana and the ectomycorrhizal fungus Laccaria bicolor: is fungal auxin the trigger? Plant Sign. Behav. 5, 864-867 (2010).

[52]

Chen, J., Jacobson, L., Handelsman, J. & Goodman, R. M. Compatibility of systemic acquired resistance and microbial biocontrol for suppression of plant diseases. Mol. Ecol. 5, 73-80 (1996).

[53]

Pasternak, T. et al. Salicylic acid affects root meristem patterning via auxin distribution in a concentration-dependent manner. Plant Physiol. 180, 1725-1739 (2019).

[54]

Gorman, N. R. & Starrett, M. C. Screening commercial peat and peat-based products for the presence of ericoid mycorrhizae. J. Environ. Hort. 21, 30-33 (2003).

[55]

Eccher, T., Piagnani, M. C. & Zordan, C. Influence of thirteen different strains of ericoid endomycorrhizae on rooting and growth of micropropagated Azalea mollis. Acta Hort. 865, 321-326 (2010).

[56]

Xiao, G. & Berch, S. M. Ericoid mycorrhizal fungi of Gaultheria shallon. Mycologia 84, 470-471 (1992).

[57]

Phillips, J. M. & Hayman, D. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158-IN118 (1970).

[58]

Šimura, J. et al. Plant hormonomics: multiple phytohormone profiling by targeted metabolomics. Plant Physiol. 177, 476-489 (2018).

[59]

Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101 (2008).

PDF (1240KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/