Abstract
Background and aims
Colonisation of roots by arbuscular mycorrhizal fungi (AMF) can increase plant biomass and nutrition under soil zinc (Zn) deficiency and toxicity conditions, but the genes and transporters involved in these processes are unknown. The aim here was to determine whether there is a ZIP (Zrt-, Irt-like protein) transporter gene that is differentially-regulated by mycorrhizal colonisation that may be involved in mycorrhizal Zn uptake.
Methods
We grew Medicago truncatula plants at soil Zn concentrations ranging from deficient to toxic, with and without inoculation of the AMF Rhizophagus irregularis, and measured plant dry weight, shoot nutrient concentrations and the expression of phosphate, aquaporin and ZIP genes in the roots.
Results
At low and high soil Zn concentrations, there were positive biomass responses to AMF colonisation. Furthermore, at low soil Zn concentrations, MtZIP6 was highly up-regulated in the mycorrhizal plants. With increasing soil Zn concentration, expression of the AMF-induced phosphate transporter gene MtPT4 increased, and mycorrhizal colonisation was maintained.
Conclusions
We have identified two different mechanisms by which AMF colonisation can increase plant biomass under low and high Zn stress: first, up-regulation of MtZIP6 at low soil Zn to supplement Zn uptake from the rhizosphere; and second, persistence of mycorrhizal colonisation and expression of MtPT4, which at high Zn could promote increased plant biomass and reduced tissue Zn concentration.
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References
Al-Karaki GN, Clark RB (1998) Growth, mineral acquisition, and water use by mycorrhizal wheat grown under water stress. J Plant Nutr 21:263–276. https://doi.org/10.1080/01904169809365401
Bowles TM, Barrios-Masias FH, Carlisle EA, Cavagnaro TR, Jackson LE (2016) Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci Total Environ 566:1223–1234. https://doi.org/10.1016/j.scitotenv.2016.05.178
Bravo A, York T, Pumplin N, Mueller LA, Harrison MJ (2016) Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat Plants 2:15208. https://doi.org/10.1038/nplants.2015.208
Bucher M, Rausch C, Daram P (2001) Molecular and biochemical mechanisms of phosphorus uptake into plants. J Plant Nutr Soil Sci 164:209–217. https://doi.org/10.1002/1522-2624(200104)164:2<209::aid-jpln209>3.0.co;2-f
Bürkert B, Robson A (1994) Zn-65 uptake in subterranean clover (Trifolium-subterraneum l) by 3 vesicular-arbuscular mycorrhizal fungi in a root-free sandy soil. Soil Biol Biochem 26:1117–1124. https://doi.org/10.1016/0038-0717(94)90133-3
Burleigh SH, Kristensen BK, Bechmann IE (2003) A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Mol Biol 52:1077–1088. https://doi.org/10.1023/a:1025479701246
Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17. https://doi.org/10.1007/s11104-007-9466-3
Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325. https://doi.org/10.1007/s11104-008-9559-7
Cavagnaro TR (2016) Soil moisture legacy effects: impacts on soil nutrients, plants and mycorrhizal responsiveness. Soil Biol Biochem 95:173–179. https://doi.org/10.1016/j.soilbio.2015.12.016
Chen BD, Li XL, Tao HQ, Christie P, Wong MH (2003) The role of arbuscular mycorrhiza in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50:839–846. https://doi.org/10.1016/s0045-6535(02)00228-x
Durmaz E et al (2011) Expression and cellular localization of ZIP1 transporter under zinc deficiency in wild emmer wheat. Plant Mol Biol Report 29:582–596. https://doi.org/10.1007/s11105-010-0264-3
Ferrol N, Tamayo E, Vargas P (2016) The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications. J Exp Bot 67:6253–6265. https://doi.org/10.1093/jxb/erw403
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Giovannetti M et al (2012) Two putative-aquaporin genes are differentially expressed during arbuscular mycorrhizal symbiosis in Lotus japonicus. BMC Plant Biol 12:186. https://doi.org/10.1186/1471-2229-12-186
Gomez SK et al (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9:10. https://doi.org/10.1186/1471-2229-9-10
Gonzalez-Guerrero M, Azcon-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42:130–140. https://doi.org/10.1016/j.fgb.2004.10.007
Gonzalez-Guerrero M, Melville LH, Ferrol N, Lott JNA, Azcon-Aguilar C, Peterson RL (2008) Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can J Microbiol 54:103–110. https://doi.org/10.1139/w07-119
Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198. https://doi.org/10.1016/S0005-2736(00)00138-3
Guether M, Neuhäuser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83. https://doi.org/10.1104/pp.109.136390
Hambidge M (2000) Human zinc deficiency. J Nutr 130:1344S–1349S
Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429. https://doi.org/10.1105/tpc.004861
Hong JJ, Park YS, Bravo A, Bhattarai KK, Daniels DA, Harrison MJ (2012) Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236:851–865. https://doi.org/10.1007/s00425-012-1677-z
Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23:481–488. https://doi.org/10.1051/agro:2003013
Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 104:1720–1725. https://doi.org/10.1073/pnas.0608136104
Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234. https://doi.org/10.1023/a:1026565701391
Khan HR, McDonald GK, Rengel Z (2003) Zn fertilization improves water use efficiency, grain yield and seed Zn content in chickpea. Plant Soil 249:389–400. https://doi.org/10.1023/a:1022808323744
Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415. https://doi.org/10.1093/pcp/pcq099
Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211:85–90. https://doi.org/10.1007/s004250000263
Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants – a meta-analysis. Soil Biol Biochem 69:123–131. https://doi.org/10.1016/j.soilbio.2013.11.001
Li S et al (2013) Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize. BMC Plant Biol 13:1–14. https://doi.org/10.1186/1471-2229-13-114
López-Millán A-F, Ellis D, Grusak M (2004) Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol Biol 54:583–596. https://doi.org/10.1023/B:PLAN.0000038271.96019.aa
Milner MJ, Seamon J, Craft E, Kochian LV (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot 64. https://doi.org/10.1093/jxb/ers315
Niemietz CM, Tyerman SD (2000) Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett 465:110–114. https://doi.org/10.1016/S0014-5793(99)01729-9
Nishida S, Mizuno T, Obata H (2008) Involvement of histidine-rich domain of ZIP family transporter TjZNT1 in metal ion specificity. Plant Physiol Biochem 46:601–606. https://doi.org/10.1016/j.plaphy.2008.02.011
Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263
Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 99:13324–13329. https://doi.org/10.1073/pnas.202474599
Pellegrino E, Öpik M, Bonari E, Ercoli L (2015) Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013. Soil Biol Biochem 84:210–217. https://doi.org/10.1016/j.soilbio.2015.02.020
Roberts DM, Routray P (2017) The Nodulin 26 intrinsic protein subfamily. In: Chaumont F, Tyerman SD (eds) Plant aquaporins: from transport to signaling. Springer, pp 267–296
Ruel MT, Bouis HE (1998) Plant breeding: a long-term strategy for the control of zinc deficiency in vulnerable populations. Am J Clin Nutr 68:488S–494S
Sagardoy R, Morales F, López-Millán AF, Abadía A, Abadía J (2009) Effects of zinc toxicity on sugar beet (Beta vulgaris L.) plants grown in hydroponics. Plant Biol 11:339–350. https://doi.org/10.1111/j.1438-8677.2008.00153.x
Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant Ionome. Annu Rev Plant Biol 59:709–733. https://doi.org/10.1146/annurev.arplant.59.032607.092942
Sarkar A, Asaeda T, Wang Q, Kaneko Y, Rashid MH (2017) Response of Miscanthus sacchariflorus to zinc stress mediated by arbuscular mycorrhizal fungi. Flora doi:https://doi.org/10.1016/j.flora.2017.05.011
Schroeder JI et al (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66. https://doi.org/10.1038/nature11909
Schüßler A, Krüger M, Walker C (2011) Revealing natural relationships among arbuscular mycorrhizal fungi: culture line BEG47 represents Diversispora epigaea, not Glomus versiforme. PLoS One 6:e23333. https://doi.org/10.1371/journal.pone.0023333
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, Third edn. Academic, New York
Stephens BW, Cook DR, Grusak MA (2011) Characterization of zinc transport by divalent metal transporters of the ZIP family from the model legume Medicago truncatula. Biometals 24:51–58. https://doi.org/10.1007/s10534-010-9373-6
Tamayo E, Gómez-Gallego T, Azcón-Aguilar C, Ferrol N (2014) Genome-wide analysis of copper, iron and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci 5:1–13. https://doi.org/10.3389/fpls.2014.00547
Uehlein N, Fileschi K, Eckert M, Bienert GP, Bertl A, Kaldenhoff R (2007) Arbuscular mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 68:122–129. https://doi.org/10.1016/j.phytochem.2006.09.033
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034.0031. https://doi.org/10.1186/gb-2002-3-7-research0034
Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007
Walder F, Brule D, Koegel S, Wiemken A, Boller T, Courty PE (2015) Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytol 205:1632–1645. https://doi.org/10.1111/nph.13292
Wallace IS, Choi W-G, Roberts DM (2006) The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim Biophys Acta 1758:1165–1175. https://doi.org/10.1016/j.bbamem.2006.03.024
Wang F, Liu X, Shi Z, Tong R, Adams CA, Shi X (2016) Arbuscular mycorrhizae alleviate negative effects of zinc oxide nanoparticle and zinc accumulation in maize plants – a soil microcosm experiment. Chemosphere 147:88–97. https://doi.org/10.1016/j.chemosphere.2015.12.076
Watts-Williams SJ, Cavagnaro TR (2012) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biol Fertil Soils 48:285–294. https://doi.org/10.1007/s00374-011-0621-x
Watts-Williams SJ, Cavagnaro TR (2014) Nutrient interactions and arbuscular mycorrhizas: a meta-analysis of a mycorrhiza-defective mutant and wild-type tomato genotype pair. Plant Soil 384:79–92. https://doi.org/10.1007/s11104-014-2140-7
Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371:299–312. https://doi.org/10.1007/s11104-013-1670-8
Watts-Williams SJ, Turney TW, Patti AF, Cavagnaro TR (2014) Uptake of zinc and phosphorus by plants is affected by zinc fertiliser material and arbuscular mycorrhizas. Plant Soil 376:165–175. https://doi.org/10.1007/s11104-013-1967-7
Watts-Williams, SJ, Jakobsen I, Cavagnaro TR, Grønlund M (2015a) Local and distal effects of arbuscular mycorrhizal colonization on direct pathway Pi uptake and root growth in Medicago truncatula. J Exp Bot 66(13):4061–4073. https://doi.org/10.1093/jxb/erv202
Watts-Williams SJ, Smith FA, McLaughlin MJ, Patti AF, Cavagnaro TR (2015b) How important is the mycorrhizal pathway for plant Zn uptake? Plant Soil 390:157–166. https://doi.org/10.1007/s11104-014-2374-4
Zhu YG, Christie P, Laidlaw AS (2001) Uptake of Zn by arbuscular mycorrhizal white clover from Zn-contaminated soil. Chemosphere 42:193–199. https://doi.org/10.1016/s0045-6535(00)00125-9
Acknowledgements
SJWW wishes to acknowledge support from the University of Adelaide Ramsay Fellowship. SJWW and SDT acknowledge support from the Australian Research Council Centre of Excellence in Plant Energy Biology (Grant number: CE140100008). We thank Prof. Mike McLaughlin for access to the ICP-AES, Mr. Antonio Coccina for comments on an earlier version of the manuscript, and Ms. Bogumila Tomczack, Ms. Wendy Sullivan, Ms. Rebecca Stonor and Mr. Antonio Coccina for technical assistance.
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Watts-Williams, S.J., Tyerman, S.D. & Cavagnaro, T.R. The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: linking plant physiology and gene expression. Plant Soil 420, 375–388 (2017). https://doi.org/10.1007/s11104-017-3409-4
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DOI: https://doi.org/10.1007/s11104-017-3409-4