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Magnesium deficiency affects secondary lignification of the vascular system in Citrus sinensis seedlings

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Mg deficiency affected only the differentiation zone in Citrus sinensis roots. Phloem impairment in Mg-deficient leaves resulted in cell wall lignifications of both vascular cambium and spongy parenchyma cells. Decrease of Mg content in the roots hampered secondary lignification of endodermal and protoxylem cell walls.

Abstract

Magnesium (Mg) is a vital nutrient for plant photosynthesis and biochemical reactions. Mg deficiency is a widespread problem in citrus production, directly affecting yield and quality. With the objective of investigating the relationship among root and leaf anatomy, photosynthetic efficiency and mineral nutrient uptake and transport in Mg-deficient citrus, the effects of Mg deficiency in ‘Xuegan’ (Citrus sinensis) seedlings on plant biomass, leaf gas exchange and chlorophyll, nutrient contents, root and leaf anatomy and lignin biosynthesis were studied. Mg deficiency decreased root and shoot dry weight, leaf CO2 assimilation, chlorophyll and Mg, phosphorus (P), boron (B), cupper (Cu) and iron (Fe) concentration in roots, stems and leaves, and increased potassium (K) and calcium (Ca) concentration. Mg deficiency in the leaves resulted in phloem disorder that blocked phloem transport, leading to carbohydrate accumulation in chloroplasts and secondary lignifications of both vascular cambium and spongy parenchyma cell walls. In contrast, decrease of Mg content in the roots hampered lignin deposition on the protoxylem and endodermal cell walls at the root differentiation zone. Poorly lignified Casparian strip and xylem cell walls in Mg-deficient root tips might decrease xylem loading efficiency of nutrients, lowering their contents in the above ground parts, which ultimately inhibited whole plant growth.

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References

  • Aitken RL, Dickson T, Hailes KJ, Moody PW (1999) Response of field-grown maize to applied magnesium in acidic soil in northeastern Australia. Aust J Agric Res 50:191–198

    Article  CAS  Google Scholar 

  • Billard V, Maillard A, Coquet L, Jouenne T, Cruz F, Garcia-Mina JM, Yvin JC, Ourry A, Etienne P (2016) Mg deficiency affects leaf Mg remobilization and the proteome in Brassica napus. Plant Physiol Biochem 107:337–343

    Article  CAS  PubMed  Google Scholar 

  • Boxler-Baldoma C, Lutz C, Heumann HG, Siefermann-Harms D (2006) Structural changes in the vascular bundles of light-exposed and shaded spruce needles suffering from Mg deficiency and ozone pollution. J Plant Physiol 163:195–205

    Article  CAS  PubMed  Google Scholar 

  • Broadley MR, White PJ (2010) Eats roots and leaves. Can edible horticultural crops address dietary calcium, magnesium and potassium deficiencies? Proc Nutr Soc 69:601–612

    Article  CAS  PubMed  Google Scholar 

  • Camacho-Cristóbal JJ, Lunar L, Lafont F, Baumert A, González-Fontes A (2004) Boron deficiency causes accumulation of chlorogenic acid and caffeoyl polyamine conjugates in tobacco leaves. J Plant Physiol 161:879–881

    Article  CAS  PubMed  Google Scholar 

  • Chapman HD (1968) The mineral nutrition of citrus. In: Reuther W, Webber HJ, Batchelor LD (eds) The citrus industry. Division of Agricultural Sciences, University of California, Davis, pp 127–189

    Google Scholar 

  • Cowan JA (2002) Structural and catalytic chemistry of magnesium-dependent enzymes. BioMetals 15:225–235

    Article  CAS  PubMed  Google Scholar 

  • Dann CE, Wakeman CA, Sieling CL, Baker SC, Irnov I, Winkler WC (2007) Structure and mechanism of a metal-sensing regulatory RNA. Cell 130:878–892

    Article  CAS  PubMed  Google Scholar 

  • Fink S (1991) Structural changes in conifer needles due to Mg and K deficiency. Fertil Res 27:23–27

    Article  CAS  Google Scholar 

  • Fischer ES, Bremer E (1993) Influence of magnesium deficiency on rates of leaf expansion, starch and sucrose accumulation and net assimilation in Phaseolus vulgaris. Physiol Plant 89:271–276

    Article  CAS  Google Scholar 

  • Guo W, Nazim H, Liang Z, Yang D (2016) Magnesium deficiency in plants: an urgent problem. Crop J 4:83–91

    Article  Google Scholar 

  • Hatfield RD, Jung HG, Ralph J, Buxtond DR, Weimera PJ (1994) A comparison of the insoluble residues produced by the Klason lignin and acid detergent lignin procedures. J Sci Food Agric 65:51–58

    Article  CAS  Google Scholar 

  • Hermans C, Johnson GN, Strasser RJ, Verbruggen N (2004) Physiological characterisation of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II. Planta 220:344–355

    Article  CAS  PubMed  Google Scholar 

  • Huang JH, Cai ZJ, Xie ZC, Li MG, Wen SX, Li J (2012) Differences of anatomic structure in citrus leaves caused by boron and magnesium deficiency. Acta Hortic Sin 39:1869–1875

    CAS  Google Scholar 

  • Huang JH, Cai ZJ, Wen SX, Guo P, Ye X, Lin GZ, Chen LS (2014) Effects of boron toxicity on root and leaf anatomy in two Citrus species differing in boron tolerance. Trees Struct Funct 28:1653–1666

    Article  CAS  Google Scholar 

  • Jin XL, Ma CL, Yang LT, Chen LS (2016) Alterations of physiology and gene expression due to long-term magnesium-deficiency differ between leaves and roots of Citrus reticulate. J Plant Physiol 198:103–115

    Article  CAS  PubMed  Google Scholar 

  • Jones DH (1984) Phenylalanine ammonia-lyase: Regulation of its induction, and its role in plant development. Phytochemistry 23:1349–1359

    Article  CAS  Google Scholar 

  • Laing W, Greer D, Sun O, Beets P, Lowe A, Payn T (2000) physiological impacts of Mg deficiency in Pinus radiate: growth and photosynthesis. New Phytol 146:47–57

    Article  CAS  Google Scholar 

  • Li Y, Han MQ, Lin F, Ten Y, Lin J, Zhu DH, Guo P, Weng YB, Chen LS (2015) Soil chemical properties, ‘Guanximiyou’ pummelo leaf mineral nutrient status and fruit quality in the southern region of Fujian province, China. J Soil Sci Plant Nutr 15:615–628

    CAS  Google Scholar 

  • Li CP, Qi YP, Zhang J, Yang LT, Wang DH, Ye X, Lai NW, Tan LL, Lin D, Chen LS (2017) Magnesium-deficiency-induced alterations of gas exchange, major metabolites and key enzymes differ among roots, lower and upper leaves of Citrus sinensis seedlings. Tree Physiol. https://doi.org/10.1093/treephys/tpx067

    Article  PubMed  Google Scholar 

  • Liang WW, Huang JH, Li CP, Yang LT, Ye X, Lin D, Chen LS (2017) MicroRNA-mediated responses to long-term magnesium-deficiency in Citrus sinensis roots revealed by Illumina sequencing. BMC Genom 18:657

    Article  CAS  Google Scholar 

  • Liao XY, Yang LT, Lu YB, Ye X, Chen LS (2015) Roles of rootstocks and scions in aluminum-tolerance of Citrus. Acta Physiol Plant 37:1743

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Ling LL, Peng LZ, Cao L, Jiang CL, Chun CP, Zhang GY, Wang ZX (2009) Effect of magnesium deficiency on photosynthesis characteristic of Beibei 447 Jinchen orange. J Fruit Sci 26:275–280

    CAS  Google Scholar 

  • Long A, Zhang J, Yang LT, Ye X, Lai NW, Tan LL, Lin D, Chen LS (2017) Effects of low pH on photosynthesis, related physiological parameters and nutrient profile of citrus. Front Plant Sci 8:185

    PubMed  PubMed Central  Google Scholar 

  • Ma CL, Qi YP, Liang WW, Yang LT, Lu YB, Guo P et al (2016) MicroRNA regulatory mechanisms on Citrus sinensis leaves to magnesium-deficiency. Front Plant Sci 7:201

    PubMed  PubMed Central  Google Scholar 

  • Marschner H (1995) Mineral nutrition in higher plants. Academic Press, San Diego

    Google Scholar 

  • Mehne-Jakobs B (1995) The influence of magnesium deficiency on carbohydrate concentrations in Norway spruce (Picea abies) needles. Tree Physiol 15:577–584

    Article  CAS  PubMed  Google Scholar 

  • Mohammadi M, Kazemi H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci 162:491–498

    Article  CAS  Google Scholar 

  • Ohno T, Grunes DL (1985) Potassium-magnesium interactions affecting nutrient uptake by wheat forage. Soil Sci Soc Am J 49:685–690

    Article  CAS  Google Scholar 

  • Peng HY, Qi YP, Lee J, Yang LT, Guo P, Jiang HX et al (2015) Proteomic analysis of Citrus sinensis roots and leaves in response to long-term magnesium-deficiency. BMC Genom 16:253

    Article  CAS  Google Scholar 

  • Puech L, Mehne-Jakobs B (1997) Histology of magnesium deficient Norway spruce needles influenced by nitrogen source. Tree Physiol 17:301–310

    Article  CAS  PubMed  Google Scholar 

  • Redgwell RJ, Hansen CE (2000) Isolation and characterisation of cell wall polysaccharides from cocoa (Theobroma cacao L.) beans. Planta 210:823–830

    Article  CAS  PubMed  Google Scholar 

  • Rottet S, Besagni C, Kessler F (2015) The role of plastoglobules in thylakoid lipid remodeling during plant development. Biochim Biophys Acta 1847:889–899

    Article  CAS  PubMed  Google Scholar 

  • Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. BioMetals 15:309–323

    Article  CAS  PubMed  Google Scholar 

  • Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2:410–418

    Article  CAS  PubMed  Google Scholar 

  • Sherson SM, Alford HL, Forbes SM, Wallace G, Smith SM (2003) Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. J Exp Bot 54:525–531

    Article  CAS  PubMed  Google Scholar 

  • Tanoi K, Kobayashi NI (2015) Leaf senescence by magnesium deficiency. Plants 4:756–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terry N, Ulrich A (1974) Effects of magnesium deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiol 54:379–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuyama T, Kawai R, Shitan N, Matoh T, Sugiyama J, Yoshinaga A, Takabe K, Fujita M, Yazaki K (2013) Proton-dependent coniferin transport, a common major transport event in differentiating xylem tissue of woody plants. Plant Physiol 162:918–926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verbruggen N, Hermans C (2013) Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant Soil 368:87–99

    Article  CAS  Google Scholar 

  • Wang MY, Wu LH, Wang WY, Liang JJ (2008) Study on common symptoms of element deficiency and concentration changes of nutrients in compositae plants. Plant Nutr Fertil Sci 14:1001–1007

    CAS  Google Scholar 

  • Wang N, Yang C, Pan Z, Liu Y, Peng SA (2015) Boron deficiency in woody plants: various responses and tolerance mechanisms. Front Plant Sci 6:916

    PubMed  PubMed Central  Google Scholar 

  • Whetten RW, MacKay JJ, Sederoff RR (1998) Recent advances in understanding lignin biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 49:585–609

    Article  CAS  PubMed  Google Scholar 

  • 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 Struct Funct 26:1237–1250

    Article  CAS  Google Scholar 

  • Yang CQ, Liu YZ, An JC, Li S, Jin LF, Zhou GF, Wei QJ, Yan HQ, Wang NN, Fu LN, Liu X, Hu XM, Yan TS, Peng SA (2013a) Digital gene expression analysis of corky split vein caused by boron deficiency in ‘Newhall’ navel orange (Citrus sinensis Osbeck) for selecting differentially expressed genes related to vascular hypertrophy. PLoS ONE 8:e65737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang LT, Yang GH, You X, Zhou XP, Lu YB, Chen LS (2013b) Magnesium deficiency-induced changes in organic acid metabolism of Citrus sinensis roots and leaves. Biol Plant 57:481–486

    Article  CAS  Google Scholar 

  • Yang C, Liu T, Bai F, Wang N, Pan Z, Yan X, Peng S (2015) MiRNAome analysis associated with anatomic and transcriptomic investigations reveal the polar exhibition of corky split vein in boron deficient Citrus sinensis. Mol Genet Genom 290:1639–1657

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the National Natural Science Foundation of China (31572081), the National Key Research and Development Program of China (2017YFD0202004), the youth talent plan of Fujian Academy of Agricultural Sciences (YC2016-3), Technology Innovation Foundation of FAAS (2016-PI37), China Agriculture Research System (CARS27), and Provincial Natural Science Foundation of Fujian, China (2016J01115 and 2016J01122).

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Authors and Affiliations

  1. Institute of Plant Nutritional Physiology and Molecular Biology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Jing-Hao Huang, Jing Xu, Xin Ye, Qiang Li & Li-Song Chen

  2. Pomological Institute, Fujian Academy of Agricultural Sciences, Fuzhou, 350013, China

    Jing-Hao Huang & Guo-Cheng Fan

  3. Central Laboratory, Fujian Academy of Agricultural Sciences, Fuzhou, 350003, China

    Tu-Yan Luo & Li-Hua Ren

  4. Institute of Materia Medica, Fujian Academy of Medical Sciences, Fuzhou, 350001, China

    Yi-Ping Qi

  5. Indian River Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, Fort Pierce, FL, 34945-3138, USA

    Rhuanito S. Ferrarezi

  6. Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Li-Song Chen

  7. The Higher Educational Key Laboratory of Fujian Province for Soil Ecosystem Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Li-Song Chen

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  1. Jing-Hao Huang
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Communicated by Sano.

The ​original ​version ​of ​this ​article ​was ​revised to update the 9th author family name.

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Huang, JH., Xu, J., Ye, X. et al. Magnesium deficiency affects secondary lignification of the vascular system in Citrus sinensis seedlings. Trees 33, 171–182 (2019). https://doi.org/10.1007/s00468-018-1766-0

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