Spatial-temporal analysis of zinc homeostasis reveals the response mechanisms to acute zinc deficiency in Sorghum bicolor

New Phytologist

Volumn 200, Issue 4, 2013, Pages 1102-1115

  Li, Yulong ^a   Zhang, Yuan ^a,b,c   Shi, Dongqing ^b   Liu, Xiaojing ^a   Qin, Jun ^d   Ge, Qing ^a   Xu, Longhua ^b   Pan, Xiangliang ^e   Li, Wei ^d   Zhu, Yiyong ^f   Xu, Jin ^a,b,c  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b KEY LABORATORY OF TROPICAL FOREST ECOLOGY   (China)

^c QINGHAI NORMAL UNIVERSITY   (China)

^d INSTITUTE OF CEREAL AND OIL CROPS   (China)

^e XINJIANG INSTITUTE OF ECOLOGY AND GEOGRAPHY   (China)

^f NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Carbonic anhydrase (CA); Copper zinc superoxide dismutase (CSD); MicroRNA; Sorghum bicolor; Zinc (Zn) deficiency

Indexed keywords

COPPER; ENZYME ACTIVITY; HOMEOSTASIS; PROTEIN; SORGHUM; SPATIOTEMPORAL ANALYSIS; ZINC;

SORGHUM BICOLOR;

ALCOHOL DEHYDROGENASE; CARBONATE DEHYDRATASE; CYCLOPENTANE DERIVATIVE; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; JASMONIC ACID; MICRORNA; OXYLIPIN; PHOSPHATE; SCAVENGER; SUPEROXIDE DISMUTASE; ZINC;

ADAPTATION; ARTICLE; BIOASSAY; CARBONIC ANHYDRASE (CA); COPPER/ZINC SUPEROXIDE DISMUTASE (CSD); DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT STOMA; REPRODUCIBILITY; SEEDLING; SORGHUM; TIME; ZINC (ZN) DEFICIENCY;

CARBONIC ANHYDRASE (CA); COPPER/ZINC SUPEROXIDE DISMUTASE (CSD); MICRORNA; SORGHUM BICOLOR; ZINC (ZN) DEFICIENCY;

ADAPTATION, PHYSIOLOGICAL; ALCOHOL DEHYDROGENASE; BASE SEQUENCE; BIOLOGICAL ASSAY; CARBONIC ANHYDRASES; CYCLOPENTANES; FREE RADICAL SCAVENGERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; INDOLEACETIC ACIDS; MICRORNAS; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; OXYLIPINS; PHOSPHATES; PHOTOSYNTHESIS; PLANT STOMATA; REPRODUCIBILITY OF RESULTS; SEEDLING; SORGHUM; SUPEROXIDE DISMUTASE; TIME FACTORS; ZINC;

EID: 84887087806     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12434     Document Type: Article

References (57)

1. Abdel-Ghany SE. 2009. Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes. Planta 229: 767-779.
2. Abdel-Ghany SE, Pilon M. 2008. MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. Journal of Biological Chemistry 283: 15932-15945.
3. Allen E, Xie Z, Gustafson AM, Carrington JC. 2005. MicroRNA directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221.
4. Alloway BJ. 2004. Zinc in soils and crop nutrition, vol. 130. Brussels, Belgium: International Zinc Association.
5. Arnon DI. 1949. Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiology 24: 1.
6. Assuncao AGL, Herrero E, Lin YF, Huettel B, Talukdar S, Smaczniak C, Immink RGH, van Eldike M, Fiers M, Schat H et al. 2010. The Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proceedings of the National Academy of Sciences, USA 107: 10296-10301.
7. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ. 2006. pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiology 141: 1000-1011.
8. Ball JT, Berry JA. 1982. The Ci/Ca ratio: a basis for predicting stomatal control of photosynthesis. Carnegie Institution of Washington Yearbook 81: 88-92.
9. Bar-Akiva A, Lavon R. 1969. Carbonic anhydrase activity as an indicator of zinc deficiency in citrus leaves. Journal of Horticultural Science 44: 359-362.
10. Beauchamp C, Fridovich I. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44: 276-287.
11. Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F. 2008. MicroRNA166 controls root and nodule development in Medicago truncatula. Plant Journal 54: 876-887.
12. Bradford M. 1976. A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
13. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A. 2007. Zinc in plants. New Phytologist 173: 677-702.
14. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL et al. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55: 611-622.
15. Cakmak I. 2000. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytologist 146: 185-205.
16. Cakmak I. 2002. Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant and Soil 247: 3-24.
17. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR et al. 2005. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Research 33: e179.
18. Dhindsa RS, Plumb-Dhindsa P, Throne TA. 1981. Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany 32: 93-101.
19. Dong J, Kim ST, Lord EM. 2005. Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiology 138: 778-789.
20. Farquhar GD, Sharkey TD. 1982. Stomatal conductance and photosynthesis. Annual Review of Plant Physiology 33: 317-345.
21. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J. 2007. Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics 39: 1033-1037.
22. Freeman JL, Tamaoki M, Stushnoff C, Quinn CF, Cappa JJ, Devonshire J, Fakra SC, Marcus MA, McGrath SP, Van Hoewyk D et al. 2010. Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiology 153: 1630-1652.
23. Gonzalez-Guerrero M, Azcón-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 Genetics and Biology 42: 130-140.
24. Hacisalihoglu G, Hart JJ, Wang Y, Cakmak I, Kochian LV. 2003. Zinc efficiency is correlated with enhanced expression and activity of Cu/Zn superoxide dismutase and carbonic anhydrase in wheat. Plant Physiology 131: 595-602.
25. Hoagland DR, Arnon DI. 1950. The water-culture for growing plants without soil. Berkeley, CA, USA: California Agricultural Experiment Station Circular 347.
26. Huang C, Barker SJ, Langridge P, Smith FW, Graham RD. 2000. Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and-deficient barley roots. Plant Physiology 124: 415-422.
27. Hwang EW, Shin SJ, Yu BK, Byun MO, Kwon HB. 2011. miR171 family members are involved in drought response in Solanum tuberosum. Journal of Plant Biology 54: 43-48.
28. Ignatova LK, Rudenko NN, Mudrik VA, Fedorchuk TP, Ivanov BN. 2011. Carbonic anhydrase activity in Arabidopsis thaliana thylakoid membrane and fragments enriched with PSI or PSII. Photosynthesis Research 110: 89-98.
29. Ilegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, Bowman JL, Stieger PA. 2010. Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 137: 975-984.
30. Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. 2005. OsZIP4, a novel zinc-regulated zinc transporter in rice. Journal of Experimental Botany 56: 3207-3214.
31. Itaya K, Ui M. 1966. A new micromethod for the colorimetric determination of inorganic phosphate. Clinica Chimica Acta 14: 361-366.
32. Jain SM, Brar DS, eds. 2010. Molecular techniques in crop improvement, 2nd edn. New York, NY, USA: Springer.
33. Jones-Rhoades MW, Bartel DP, Bartel B. 2006. MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 57: 19-53.
34. Lacombe S, Nagasaki H, Santi C, Duval D, Piegu B, Bangratz M, Breitler J-C, Guiderdoni E, Brugidou C, Hirsch J et al. 2008. Identification of precursor transcripts for 6 novel miRNAs expands the diversity on the genomic organisation and expression of miRNA genes in rice. BMC Plant Biology 8: 123.
35. Li X, Bonawitz ND, Weng JK, Chapple C. 2010. The growth reduction associated with repressed lignin biosynthesis in Arabidopsis thaliana is independent of flavonoids. Plant Cell 22: 1620-1632.
36. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ. 2008. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiology 147: 732-746.
37. Loneragan JF, Webb MJ. 1993. Interactions between zinc and other nutrients affecting the growth of plants. In: Robson AD, ed. Zinc in soils and plants. Dordrecht, the Netherlands: Kluwer Academic Publishers, 119-134.
38. Ma HS, Liang D, Shuai P, Xia XL, Yin WL. 2010. The salt- and drought inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. Journal of Experimental Botany 61: 4011-4019.
39. Marschner H. 1995. Mineral nutrition of higher plants, 2nd edn. London, UK: Academic Press.
40. Nanjo Y, Skultety L, Ashraf Y, Komatsu S. 2010. Comparative proteomic analysis of early-stage soybean seedlings responses to flooding by using gel and gel-free techniques. Journal of Proteome Research 9: 3989-4002.
41. Nersissian AM, Valentine JS, Immoos C, Hill MG, Hart PJ, Williams G, Herrmann RG. 1998. Uclacyanins, stellacyanins, and plantacyanins are distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Science 7: 1915-1929.
42. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR. 2009. Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time PCR profiling and small RNA sequencing. Plant Physiology 150: 1541-1555.
43. Qi X, Zhang Y, Chai T. 2007. Characterization of a novel plant promoter specifically induced by heavy metal and identification of the promoter regions conferring heavy metal responsiveness. Plant Physiology 143: 50-59.
44. Randall PJ, Bouma D. 1973. Zinc deficiency, carbonic anhydrase, and photosynthesis in leaves of spinach. Plant Physiology 52: 229-232.
45. Ravet K, Danford FL, Dihle A, Pittarello M, Pilon M. 2011. Spatial-temporal analysis of Cu homeostasis in Populus trichocarpa reveals an integrated molecular remodeling for a preferential allocation of copper to plastocyanin in the chloroplasts of developing leaves. Plant Physiology 157: 1300-1312.
46. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D. 2005. Specific effects of microRNAs on the plant transcriptome. Development Cell 8: 517-527.
47. Sharma PN, Kumar P, Tewari RK. 2004. Early signs of oxidative stress in wheat plants subjected to zinc deficiency. Journal of Plant Nutrition 27: 451-463.
48. Song C, Fang J, Li X, Liu H, Thomas Chao C. 2009. Identification and characterization of 27 conserved microRNAs in citrus. Planta 230: 671-685.
49. Song CN, Wang C, Zhang CQ, Nicholas KK, Yu HP, Ma ZQ, Fang JG. 2010. Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genomics 11: 431.
50. Wissuwa M, Ismail AM, Yanagihara S. 2006. Effects of zinc deficiency on rice growth and genetic factors contributing to tolerance. Plant Physiology 142: 731-741.
51. Xie ZX, Duan LS, Tian XL, Wang BM, Eneji AE, Li ZH. 2008. Coronatine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. Journal of Plant Physiology 165: 375-384.
52. Xu J, Yin HX, Li YL, Liu XJ. 2010. Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiology 154: 1319-1334.
53. Yang J, Zhang J, Wang Z, Zhu Q, Wang W. 2001. Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiology 127: 315-323.
54. Yin CY, Berninger F, Li CY. 2006. Photosynthetic responses of Populus przewalski subjected to drought stress. Photosynthetica 44: 62-68.
55. Yu Q, Rengel Z. 1999. Micronutrient deficiency influences plant growth and activities of superoxide dismutases in narrow-leafed lupins. Annals of Botany 83: 175-182.
56. Zhang ZX, Wei LY, Zou XL, Tao YS, Liu ZJ, Zheng YL. 2008. Submergence-responsive microRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Annals of Botany 102: 509-519.
57. Zhong R, Ye ZH. 2001. Alteration of auxin polar transport in the Arabidopsis ifl1 mutants. Science Signalling 126: 549.