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Mycorrhiza alters the profile of root hairs in trifoliate orange

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Abstract

Root hairs and arbuscular mycorrhiza (AM) coexist in root systems for nutrient and water absorption, but the relation between AM and root hairs is poorly known. A pot study was performed to evaluate the effects of four different AM fungi (AMF), namely, Claroideoglomus etunicatum, Diversispora versiformis, Funneliformis mosseae, and Rhizophagus intraradices on root hair development in trifoliate orange (Poncirus trifoliata) seedlings grown in sand. Mycorrhizal seedlings showed significantly higher root hair density than non-mycorrhizal seedlings, irrespective of AMF species. AMF inoculation generally significantly decreased root hair length in the first- and second-order lateral roots but increased it in the third- and fourth-order lateral roots. AMF colonization induced diverse responses in root hair diameter of different order lateral roots. Considerably greater concentrations of phosphorus (P), nitric oxide (NO), glucose, sucrose, indole-3-acetic acid (IAA), and methyl jasmonate (MeJA) were found in roots of AM seedlings than in non-AM seedlings. Levels of P, NO, carbohydrates, IAA, and MeJA in roots were correlated with AM formation and root hair development. These results suggest that AMF could alter the profile of root hairs in trifoliate orange through modulation of physiological activities. F. mosseae, which had the greatest positive effects, could represent an efficient AM fungus for increasing fruit yields or decreasing fertilizer inputs in citrus production.

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References

  • Assaad FF (2009) The membrane dynamics of root hair morphogenesis. In: Emons AMC, Ketelaar T (eds) Root hairs. Springer, Berlin, pp 65–84

    Chapter  Google Scholar 

  • Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y (2003) Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol 131:1496–1507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnola LG, Montilla MG (1997) Vertical distribution of mycorrhizal colonization, root hairs, and belowground biomass in three contrasting sites from the tropical high mountains, Merida, Venezuela. Arct Alp Res 29:206–212

    Article  Google Scholar 

  • Baylis GTS (1975) The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In: Sanders FE, Mosse B, Tinker PB (eds) Endomycorrhizas. Academic, London, pp 373–389

    Google Scholar 

  • Bray DF, Bagu J, Koegler P (1993) Comparison of hexamethyldisilazane (HMDS), Peldri II, and critical-point drying methods for scanning electron microscopy of biological specimens. Microsc Res Tech 26:489–495

    Article  CAS  PubMed  Google Scholar 

  • Brown LK, George TS, Barrett GE, Hubbard SF, White PJ (2013a) Interactions between root hair length and arbuscular mycorrhizal colonisation in phosphorus deficient barley (Hordeum vulgare). Plant Soil 372:195–205

    Article  CAS  Google Scholar 

  • Brown LK, George TS, Dupuy LX, White PJ (2013b) A conceptual model of root hair ideotypes for future agricultural environments: what combination of traits should be targeted to cope with limited P availability? Ann Bot 112:317–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calcagno C, Novero M, Genre A, Bonfante P, Lanfranco L (2012) The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncata roots. Mycorrhiza 22:259–269

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Chen CL, Zhang DJ, Shu B, Xiao J, Xia RX (2013) Influence of nutrient deficiency on root architecture and root hair morphology of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings under sand culture. Sci Hortic 162:100–105

    Article  CAS  Google Scholar 

  • Caradus JR (1981) Effect of root hair length on white clover growth over a range of soil phosphorus levels. N Z J Agric Res 24:353–358

    Article  Google Scholar 

  • Chen Q, Qi WB, Reiter RJ, Wei W, Wang BM (2009) Exogenously applied melatonin stimulates root growth and raises endogenous indoleacetic acid in roots of etiolated seedlings of Brassica juncea. J Plant Physiol 166:324–328

    Article  CAS  PubMed  Google Scholar 

  • Cheng YW, Zhu WJ, Chen YX, Ito S, Asami T, Wang XL (2014) Brassinosteroids control root epidermal cell fate via direct regulation of a MYB-bHLH-WD40 complex by GSK3-like kinases. Elife. 3:e02525. doi:10.7554/eLife.02525

  • Espinosa F, Garrido I, Ortega A, Casimiro I, Álvarez-Tinaut MC (2014) Redox activities and ROS, NO and phenylpropanoids production by axenically cultured intact olive seedling roots after interaction with a mycorrhizal or a pathogenic fungus. PLoS One 9:e100132

    Article  PubMed  PubMed Central  Google Scholar 

  • Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 110:E5025–E5034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foo E (2013) Auxin influences strigolactones in pea mycorrhizal symbiosis. J Plant Physiol 170:523–528

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Ross JJ, Jones WT, Reid JB (2013) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111:769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruszka D (2013) The brassinosteroid signaling pathway – New key players and interconnections with other signaling networks crucial for plant development and stress tolerance. Int J Mol Sci 14:8740–8774

    Article  PubMed  PubMed Central  Google Scholar 

  • Guinel FC, Hirsch AM (2000) The involvement of root hairs in mycorrhizal associations. In: Ridge RW, Emons AMC (eds) Root hairs. Springer, Tokyo, pp 285–310

    Chapter  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill JO, Simpson RJ, Ryan MH, Chapman DF (2010) Root hair morphology and mycorrhizal colonisation of pasture species in response to phosphorus and nitrogen nutrition. Crop Pasture Sci 61:122–131

    Article  CAS  Google Scholar 

  • Izumo M, Ridge RW, Katsumi M (1995) Honnonal control of root hair growth in clover. In: Abstracts of the 15th International Conference on Plant Growth Substances, Minneapolis, MN., p 452

    Google Scholar 

  • Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphorus starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145:1460–1470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katsumi M, Izumo M, Ridge RW (2000) Hormonal control of root hair growth and development. In: Ridge RW, Emons AMC (eds) Root hairs. Springer, Tokyo, pp 101–114

    Chapter  Google Scholar 

  • Kitson RE, Mellon MG (1944) Colorimetric determination of phosphorus as molydivanado phosphoric acid. Ind Eng Chem Anal Ed 16:379

    Article  CAS  Google Scholar 

  • Kühn C, Grof CPL (2010) Sucrose transporters of higher plants. Curr Opin Plant Biol 13:288–298

    Article  PubMed  Google Scholar 

  • Kwasniewski M, Chwialkowska K, Kwasniewska J, Kusak J, Siwinski K, Szarejko I (2013) Accumulation of peroxidase-related reactive oxygen species in trichoblasts correlates with root hair initiation in barley. J Plant Physiol 170:85–195

    Article  Google Scholar 

  • Lamont B (1983) Root hair dimensions and surface/volume/weight ratios of roots with the aid of scanning electron microscopy. Plant Soil 74:149–152

    Article  Google Scholar 

  • Lee SH, Cho HT (2008) Auxin and root hair morphogenesis. In: Emons AMC, Ketelaar T (eds) Root hairs. Springer, Berlin, pp 45–64

    Google Scholar 

  • Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33

    Article  PubMed  PubMed Central  Google Scholar 

  • Ludwig-Müller J (2010) Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer Science + Business Media B.V, New York, pp 169–196

    Chapter  Google Scholar 

  • Maherali H (2014) Is there an association between root architecture and mycorrhizal growth response? New Phytol 204:192–200

    Article  PubMed  Google Scholar 

  • Manjunath A, Habte M (1991) Root morphological characteristics of host species having distinct mycorrhizal dependency. Can J Bot 69:671–676

    Article  Google Scholar 

  • Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715

    Article  CAS  PubMed  Google Scholar 

  • Mishra BS, Singh M, Aggrawal P, Laxmi A (2009) Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS One 4:e4502

    Article  PubMed  PubMed Central  Google Scholar 

  • Novero M, Genre A, Szczyglowski K, Bonfante P (2008) Root hair colonization by mycorrhizal fungi. In: Emons AMC, Ketelaar T (eds) Root hairs. Springer, Berlin, pp 315–338

    Google Scholar 

  • Orfanoudakis M, Wheeler CT, Hooker JE (2010) Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 20:117–126

    Article  PubMed  Google Scholar 

  • Pei WK, Du F, Zhang Y, He T, Ren HY (2012) Control of the actin cytoskeleton in root hair development. Plant Sci 187:10–18

    Article  CAS  PubMed  Google Scholar 

  • Peterson RL (1992) Adaptions of root structure in relation to biotic and abiotic factors. Can J Bot 70:661–675

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K, Hatzopoulos P (2013) Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol 197:1130–1141

    Article  CAS  PubMed  Google Scholar 

  • Shaul-Keinan O, Gadkar V, Ginzberg I, Grünzweig JM, Chet I, Elad Y, Wininger S, Belausov E, Eshed Y, Atzmon N, Ben-Tal Y, Kapulnik Y (2002) Hormone concentrations in tobacco roots change during arbuscular mycorrhizal colonization with Glomus intraradices. New Phytol 154:501–507

    Article  CAS  Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun XG, Tang M (2013) Effect of arbuscular mycorrhizal fungi inoculation on root traits and root volatile organic compound emissions of Sorghum bicolor. South Afr J Bot 88:373–379

    Article  CAS  Google Scholar 

  • Takeda N, Handa Y, Tsuzuki S, Kojima M, Sakakibara H, Kawaguchi M (2015) Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus. Plant Physiol 167:545–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu QS, Srivastava AK, Li Y (2015) 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

    Article  CAS  Google Scholar 

  • Wu QS, Srivastava AK, Zou YN (2013a) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, Huang YM, Li Y, He XH (2013b) Arbuscular mycorrhizal fungi induce sucrose cleavage for carbon supply of arbuscular mycorrhizas in citrus genotypes. Sci Hortic 160:320–325

    Article  CAS  Google Scholar 

  • Yao Q, Zhu HH, Chen JZ (2005) Growth responses and endogenous IAA and iPAS changes of litchi (Litchi chinensis Sonn.) seedlings induced by arbuscular mycorrhizal fungal inoculation. Sci Hortic 105:145–151

    Article  CAS  Google Scholar 

  • Zhang DJ, Xia RX, Cao X, Shu B, Chen CL (2013) Root hair development of Poncirus trifoliata grown in different growth cultures and treated with 3-indolebutyric acid and ethephon. Sci Hortic 160:389–397

    Article  CAS  Google Scholar 

  • Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54:2351–2361

    Article  CAS  PubMed  Google Scholar 

  • Zhu CH, Gan LJ, Shen ZG, Xia K (2006) Interactions between jasmonates and ethylene in the regulation of root hair development in Arabidopsis. J Exp Bot 57:1299–1308

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Foundation of China (31372017), the Open Fund of Institute of Root Biology, Yangtze University (R201401), and the Project of Excellence FIM UHK.

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Authors and Affiliations

  1. College of Horticulture and Gardening, Yangtze University, Jingzhou, 434025, Hubei, People’s Republic of China

    Qiang-Sheng Wu, Chun-Yan Liu, De-Jian Zhang & Ying-Ning Zou

  2. Institute of Root Biology, Yangtze University, Jingzhou, 434025, Hubei, People’s Republic of China

    Qiang-Sheng Wu, Chun-Yan Liu, De-Jian Zhang & Ying-Ning Zou

  3. School of Plant Biology, University of Western Australia, Crawley, WA, 6009, Australia

    Xin-Hua He

  4. Department of Environmental Sciences, University of Sydney, Eveleigh, NSW, 2015, Australia

    Xin-Hua He

  5. Center for Basic and Applied Research, Faculty of Informatics and Management, University of Hradec Kralove, Hradec Kralove, Czech Republic

    Qing-Hua Wu

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  1. Qiang-Sheng Wu
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Correspondence to Qiang-Sheng Wu.

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Wu, QS., Liu, CY., Zhang, DJ. et al. Mycorrhiza alters the profile of root hairs in trifoliate orange. Mycorrhiza 26, 237–247 (2016). https://doi.org/10.1007/s00572-015-0666-z

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