Key message
At least eight MGT genes were identified in citrus and PtrMGT5 plays important role in maintaining Mg homeostasis in citrus by getting involved in the Mg absorption and transport.
Abstract
Magnesium (Mg) is an essential macronutrient for plant growth and development, and the magnesium transporter (MGT) genes participate in mediate Mg2+ uptake, translocation and sequestration into cellular storage compartments. Although several MGT genes have been characterized in various plant species, a comprehensive analysis of the MGT gene family in citrus is still uncharacterized. In this study, eight PtrMGT genes were identified through genome-wide analyses. Phylogenetic analyses revealed that PtrMGT genes were classified into five distinct subfamilies. A quantitative RT-PCR analysis showed that eight PtrMGT genes were expressed in all of the detected tissues and they mainly expressed in the vegetative organs. Expression analyses revealed the PtrMGT genes responded to various Mg deficiency stresses, including absolute Mg deficiency and antagonistic Mg deficiency which caused by low pH or Al toxicity. PtrMGT5, which localizes to the plasma membrane and was transcriptionally active, was functionally characterized. PtrMGT5 overexpression considerably enhanced absolute Mg deficiency and antagonistic Mg deficiency tolerance in transgenic Arabidopsis plants, which was accompanied by increased fresh weight and Mg content, whereas opposite changes were observed when PtrMGT5 homolog in Valencia Orange callus was knocked down. Taken together, PtrMGT5 plays important role in maintaining Mg homeostasis in citrus by getting involved in the Mg absorption and transport.
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References
Aitken RL, Dickson T, Hailes KJ, Moody PW, Aitken RL, Dickson T, Hailes KJ, Moody PW (1999) Response of field-grown maize to applied magnesium in acidic soils in north-eastern Australia. Aust J Agric Res 50:191–198
Bennett WF (1993) Nutrient deficiencies and toxicities in crop plants. APS Press, St. Paul
Bose J, Babourina O, Shabala S, Rengel Z (2013) Low-pH and aluminum resistance in arabidopsis correlates with high cytosolic magnesium content and increased magnesium uptake by plant roots. Plant Cell Physiol 54:1093–1104
Cakmak I, Yazi̇Ci̇ AM (2010) Magnesium: a forgotten element in crop production. Better Crops Plant Food 94:23–25
Ceylan Y, Kutman UB, Mengutay M, Cakmak I (2016) Magnesium applications to growth medium and foliage affect the starch distribution, increase the grain size and improve the seed germination in wheat. Plant Soil 406:145–156
Chen ZC, Ma JF (2012) Magnesium transporters and their role in Al tolerance in plants. Plant Soil 368:51–56
Chen ZC, Yamaji N, Motoyama R, Nagamura Y, Ma JF (2012) Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice. Plant Physiol 159:1624–1633
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469
Eshaghi S, Niegowski D, Kohl A, Martinez Molina D, Lesley SA, Nordlund P (2006) Crystal structure of a divalent metal ion transporter CorA at 2.9 angstrom resolution. Science 313:354–357
Farhat N, Elkhouni A, Zorrig W, Smaoui A, Abdelly C, Rabhi M (2016) Effects of magnesium deficiency on photosynthesis and carbohydrate partitioning. Acta Physiol Plant 38:145
Gebert M, Meschenmoser K, Svidova S, Weghuber J, Schweyen R, Eifler K, Lenz H, Weyand K, Knoop V (2009) A root-expressed magnesium transporter of the MRS2/MGT gene family in Arabidopsis thaliana allows for growth in low-Mg2+ environments. Plant Cell 21:4018–4030
Gransee A, Führs H (2013) Magnesium mobility in soils as a challenge for soil and plant analysis, magnesium fertilization and root uptake under adverse growth conditions. Plant Soil 368:5–21
Grauer UE (1993) Modelling anion amelioration of aluminium phytotoxicity. Plant Soil 157:319–331
Grzebisz W (2011) Magnesium-food and human health. J Elementol 16:299–323
Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Møller IS, White P (2012) Functions of macronutrients. Pergamon, London
Hermans C, Bourgis F, Faucher M, Strasser RJ, Delrot S, Verbruggen N (2005) Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves. Planta 220:541–549
Hirano Y, Hijii N (1998) Effects of low pH and aluminum on root morphology of Japanese red cedar saplings. Environ Pollut 101:339–347
Kenneth J, Livak TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2△△ct method. Method 25(4):402–408
Kurusu T, Nishikawa D, Yamazaki Y, Gotoh M, Nakano M, Hamada H, Yamanaka T, Iida K, Nakagawa Y, Saji H (2012) Plasma membrane protein OsMCA1 is involved in regulation of hypo-osmotic shock-induced Ca2+ influx and modulates generation of reactive oxygen species in cultured rice cells. BMC Plant Biol 12:11
Li L, Tutone AF, Drummond RS, Gardner RC, Luan S (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13:2761–2775
Li SB, Ouyang WZ, Hou XJ, **e LL, Hu CG, Zhang JZ (2015) Genome-wide identification, isolation and expression analysis of auxin response factor (ARF) gene family in sweet orange (Citrus sinensis). Frontiers in Plant Science 6:119
Li H, Du H, Huang K, Chen X, Liu T, Gao S, Liu H, Tang Q, Rong T, Zhang S (2016) Identification, and functional and expression analyses of the CorA/MRS2/MGT-type magnesium transporter family in maize. Plant Cell Physiol 57:1153–1168
Liu YZ, Liu Q, Tao NG, Deng XX (2006) Efficient isolation of RNA from fruit peel and pulp of ripening navel orange (Citrus sinensis Osbeck). J Huazhong Agri Univ 25(3):300–304
Lunin VV, Dobrovetsky E, Khutoreskaya G, Zhang R, Joachimiak A, Doyle DA, Bochkarev A, Maguire ME, Edwards AM, Koth CM (2006) Crystal structure of the CorA Mg2+ transporter. Nature 440:833
Mao D, Chen J, Tian L, Liu Z, Yang L, Tang R, Li J, Lu C, Yang Y, Shi J, Chen L, Li D, Luan S (2014) Arabidopsis transporter MGT6 mediates magnesium uptake and is required for growth under magnesium limitation. Plant Cell 26:2234–2248
Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Elsevier, Amsterdam
Maselli GA, Mora-García S (2014) Revisiting the evolutionary history and roles of protein phosphatases with Kelch-like domains in plants. Plant Physiol 164:1527–1541
Mitchell AD, Loganathan P, Payn TW, Tillman RW, Mitchell AD, Loganathan P, Payn TW, Tillman RW (1999) Effect of calcined magnesite on soil and Pinus radiata foliage magnesium in pumice soils of New Zealand. Soil Res 37(3):545–560
Peng HY, Qi YP, Lee J, Yang LT, Guo P, Jiang HX, Chen LS (2015) Proteomic analysis of Citrus sinensis roots and leaves in response to long-term magnesium-deficiency. BMC Genom 16:253
Saito T, Kobayashi NI, Tanoi K, Iwata N, Suzuki H, Iwata R, Nakanishi TM (2013) Expression and functional analysis of the CorA-MRS2-ALR-type magnesium transporter family in rice. Plant Cell Physiol 54:1673–1683
Schock I, Gregan J, Steinhauser S, Schweyen R, Brennicke A, Knoop V (2000) A member of a novel Arabidopsis thaliana gene family of candidate Mg2+ ion transporters complements a yeast mitochondrial group II intron-splicing mutant. Plant J 24:489–501
Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:307–321
Tang N, Li Y, Chen LS (2012) Magnesium deficiency–induced impairment of photosynthesis in leaves of fruiting Citrus reticulata trees accompanied by up-regulation of antioxidant metabolism to avoid photo-oxidative damage. J Plant Nutr Soil Sci 175:784–793
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Yang GH, Yang LT, Jiang HX, Li Y, Wang P, Chen LS (2012) Physiological impacts of magnesium-deficiency in Citrus seedlings: photosynthesis, antioxidant system and carbohydrates. Trees 26:1237–1250
Zhou GF, Peng SA, Liu YZ, Wei QJ, Han J, Islam MZ (2014) The physiological and nutritional responses of seven different citrus rootstock seedlings to boron deficiency. Trees 28:295–307
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This work was supported by the earmarked fund for China Agriculture Research System (CARS-26).
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X.L., YZ.L., and SA.P. designed the experiments and wrote the paper. X.L., LX.G and LJ.L performed the experiments and analyzed the data.
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Liu, X., Guo, LX., Luo, LJ. et al. Identification of the magnesium transport (MGT) family in Poncirus trifoliata and functional characterization of PtrMGT5 in magnesium deficiency stress. Plant Mol Biol 101, 551–560 (2019). https://doi.org/10.1007/s11103-019-00924-9
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DOI: https://doi.org/10.1007/s11103-019-00924-9