The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: linking plant physiology and gene expression
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.
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.
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.
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.
KeywordsAquaporin Arbuscular mycorrhizal fungi Medicago truncatula Phosphate transporter Rhizophagus irregularis Zinc ZIP transporter
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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
- 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 267–296Google Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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
- Smith SE, Read DJ (2008) Mycorrhizal symbiosis, Third edn. Academic, New YorkGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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