Identification of manganese-toxicity-responsive genes in roots of two citrus species differing in manganese tolerance using cDNA-AFLP

Published Date
June 2017, Volume 31, Issue 3, pp 813–831

Author

• Chen-Ping Zhou
• Chun-Ping Li
• Wei-Wei Liang
• Peng Guo
• Lin-Tong Yang
• Li-Song ChenEmail author

1. 1.
2. 2.
3. 3.

Original Article

First Online: 

18 December 2016

Abstract

Key message

We identified more Mn-toxicity-responsive genes from Mn-intolerantCitrus grandisthan from Mn-tolerantCitrus sinensisroots. These findings increased our understanding of the molecular mechanisms on plant Mn toxicity and Mn tolerance.

Abstract

Manganese (Mn) toxicity is the most important factor limiting crop production after aluminum toxicity in acidic soils. However, little is known about Mn-toxicity-induced alterations of gene expression profiles in woody plants. Using cDNA-AFLP, we identified 87 and 63 Mn-toxicity-responsive genes from Mn-intolerant ‘Sour pummelo’ (Citrus grandis) and Mn-tolerant ‘Xuegan’ (Citrus sinensis) roots. Among these genes, only 22 genes with the same accession number were shared by both. Protein phosphorylation/dephosphorylation-related genes were upregulated in C. sinensis roots, and downregulated in C. grandis roots except for one differentially expressed gene. Sulfur metabolism-related genes were repressed only in Mn-toxic C. grandis roots. Obviously, great differences existed in Mn-toxicity-induced alterations of gene expression profiles between C. sinensis and C. grandis roots. Genes related to protein phosphorylation/dephosphorylation (i.e., cyclin-dependent kinase-activating kinase assembly factor-related protein and PP2A regulatory subunit TAP46), cellular transport (i.e., Ca-transporting ATPase 1), and nucleic acid (i.e., ethylene-responsive transcription factor ERF109-like, structural maintenance of chromosomes protein 4-like, RNA-binding protein and DEAD-box ATP-dependent RNA helicase 21), cell wall (i.e., pectin methylesterase 1 and invertase/pectin methylesterase inhibitor family protein) and fatty acid (i.e., carboxylesterase 20) metabolisms might play a role in C. sinensis Mn tolerance. In addition, cell wall materials were increased in Mn-toxic C. sinensis and C. grandis roots, especially in the former. Interestingly, lignin content was increased in Mn-toxic C. sinensis roots, while a reverse trend was displayed in Mn-toxic C. grandis roots. In conclusion, our results provided novel clues to the molecular mechanisms on Mn toxicity and Mn tolerance in higher plants.

Keywords

cDNA-AFLP Cell wall Citrus grandis Citrus sinensis Manganese toxicity Root gene expression 

Communicated by R. Alia.

Electronic supplementary material

The online version of this article (doi:10.1007/s00468-016-1507-1) contains supplementary material, which is available to authorized users.

Supplementary material

468_2016_1507_MOESM1_ESM.docx (23 kb)

Supplementary material 1 (DOCX 23 kb)

References

1. Alam S, Kamei S, Kawai S (2000) Phytosiderophore release from manganese induced iron deficiency in barley. J Plant Nutr 23:1193–1207CrossRefGoogle Scholar
2. Ali MA, Plattner S, Radakovic Z, Wieczorek K, Elashry A, Grundler FM, Ammelburg M, Siddique S, Bohlmann H (2013) An Arabidopsis ATPase gene involved in nematode-induced syncytium development and abiotic stress responses. Plant J 74:852–866CrossRefPubMedPubMedCentralGoogle Scholar
3. Ambrosone A, Batelli G, Nurcato R, Aurilia V, Punzo P, Bangarusamy DK, Ruberti I, Sassi M, Leone A, Costa A, Grillo S (2015) The Arabidopsis RNA-binding protein AtRGGA regulates tolerance to salt and drought stress. Plant Physiol 168:292–306CrossRefPubMedPubMedCentralGoogle Scholar
4. An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228:61–78CrossRefPubMedPubMedCentralGoogle Scholar
5. Armstrong FA (2008) Why did nature choose manganese to make oxygen? Philos Trans R Soc B Lond B Biol Sci 363:1263–1270CrossRefGoogle Scholar
6. Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3across membranes. BMC Biol 6:26CrossRefPubMedPubMedCentralGoogle Scholar
7. Bischoff V, Nita S, Neumetzler L, Schindelasch D, Urbain A, Eshed R, Persson S, Delmer D, Scheible WR (2010) TRICHOME BIREFRINGENCE and its homolog AT5G01360 encode plant-specific DUF231 proteins required for cellulose biosynthesis in Arabidopsis. Plant Physiol 153:590–602CrossRefPubMedPubMedCentralGoogle Scholar
8. Boojar MMA, Goodarzi F (2008) Comparative evaluation of oxidative stress status and manganese availability in plants growing on manganese mine. Ecotoxicol Environ Safe 71:692–699CrossRefGoogle Scholar
9. Boycheva I, Vassileva V, Iantcheva A (2014) Histone acetyltransferases in plant development and plasticity. Curr Genom 15:28–37CrossRefGoogle Scholar
10. Chen Z, Sun L, Liu P, Liu G, Tian J, Liao H (2015) Malate synthesis and secretion mediated by a manganese-enhanced malate dehydrogenase confers superior manganese tolerance in Stylosanthes guianensis. Plant Physiol 167:176–188CrossRefPubMedGoogle Scholar
11. Chen Z, Yan W, Sun L, Tian J, Liao H (2016) Proteomic analysis reveals growth inhibition of soybean roots by manganese toxicity is associated with alteration of cell wall structure and lignification. J Proteom 143:151–160CrossRefGoogle Scholar
12. Cnops G, Neyt P, Raes J, Petrarulo M, Nelissen H, Malenica N, Luschnig C, Tietz O, Ditengou F, Palme K, Azmi A, Prinsen E, Van Lijsebettens M (2006) The TORNADO1 and TORNADO2 genes function in several patterning processes during early leaf development in Arabidopsis thaliana. Plant Cell 18:852–866CrossRefPubMedPubMedCentralGoogle Scholar
13. Craciun AR, Courbot M, Bourgis F, Salis P, Saumitou-Laprade P, Verbruggen N (2006) Comparative cDNA-AFLP analysis of Cd-tolerant and -sensitive genotypes derived from crosses between the Cd hyperaccumulator Arabidopsis halleri and Arabidopsis lyrata ssp. petraea. J Exp Bot 57:2967–2983CrossRefPubMedGoogle Scholar
14. El-Moneim DA, Contreras R, Silva-Navas J, Gallego FJ, Figueiras AM, Benito C (2014) Pectin methylesterase gene and aluminum tolerance in Secale cereale. Environ Exp Bot 107:125–133CrossRefGoogle Scholar
15. Ernst WH, Krauss GJ, Verkleij JA, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143PubMedGoogle Scholar
16. Falcone A, Nelissen H, Fleury D, Van Lijsebettens M, Bitonti MB (2007) Cytological investigations of the Arabidopsis thaliana elol mutant give new insights into leaf lateral growth and elongator function. Ann Bot 100:261–270CrossRefPubMedPubMedCentralGoogle Scholar
17. Fan W, Lou HQ, Gong YL, Liu MY, Wang ZQ, Yang JL, Zheng SJ (2014) Identification of early Al-responsive genes in rice bean (Vigna umbellata) roots provides new clues to molecular mechanisms of Al toxicity and tolerance. Plant Cell Environ 37:1586–1597CrossRefPubMedGoogle Scholar
18. Führs H, Hartwig M, Molina LE, Heintz D, Van Dorsselaer A, Braun HP, Horst WJ (2008) Early manganese-toxicity response in Vigna unguiculata L.—a proteomic and transcriptomic study. Proteomics 8:149–159CrossRefPubMedGoogle Scholar
19. Fusco N, Micheletto L, Dal Corso G, Borgato L, Furini A (2005) Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L. J Exp Bot 56:3017–3027CrossRefPubMedGoogle Scholar
20. Gendra E, Moreno A, Alba MM, Pages M (2004) Interaction of the plant glycine-rich RNA-binding protein MA16 with a novel nucleolar DEAD box RNA helicase protein from Zea mays. Plant J 38:875–886CrossRefPubMedGoogle Scholar
21. Gershater MC, Edwards R (2007) Regulating biological activity in plants with carboxylesterases. Plant Sci 173:579–588CrossRefGoogle Scholar
22. Gichner T, Patková Z, Száková J, Demnerová K (2006) Toxicity and DNA damage in tobacco and potato plants growing on soil polluted with heavy metals. Ecotoxicol Environ Safe 65:420–426CrossRefGoogle Scholar
23. Gupta OP, Sharma P, Gupta RK, Sharma I (2014) MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives. Plant Mol Biol 84:1–18CrossRefPubMedGoogle Scholar
24. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11CrossRefPubMedGoogle Scholar
25. Hatfield RD, Jung HG, Ralph J, Buxton DR, Weimer PJ (1994) A comparison of the insoluble residues produced by the Klason lignin and acid detergent lignin procedures. J Sci Food Agric 65:51–58CrossRefGoogle Scholar
26. Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611CrossRefGoogle Scholar
27. Hossain Z, Komatsu S (2013) Contribution of proteomic studies towards understanding plant heavy metal stress response. Front Plant Sci 3:310CrossRefPubMedPubMedCentralGoogle Scholar
28. Ileperuma NR, Marshall SD, Squire CJ, Baker HM, Oakeshott JG, Russell RJ, Plummer KM, Newcomb RD, Baker EN (2007) High-resolution crystal structure of plant carboxylesterase AeCXE1, from Actinidia eriantha, and its complex with a high-affinity inhibitor paraoxon. Biochemistry 46:1851–1859CrossRefPubMedGoogle Scholar
29. Jiang SC, Mei C, Liang S, Yu YT, Lu K, Wu Z, Wang XF, Zhang DP (2015) Crucial roles of the pentatricopeptide repeat protein SOAR1 in Arabidopsis response to drought, salt and cold stresses. Plant Mol Biol 88:369–385CrossRefPubMedPubMedCentralGoogle Scholar
30. Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M, Fujiwara T (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284:2114–2120CrossRefPubMedGoogle Scholar
31. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260CrossRefGoogle Scholar
32. Kovácik J, Klejdus B (2008) Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots. Plant Cell Rep 27:605–615CrossRefPubMedGoogle Scholar
33. Kushwaha A, Rani R, Kumar S, Gautam A (2015) Heavy metal detoxification and tolerance mechanisms in plants: implications for phytoremediation. Environ Rev 24:39–51CrossRefGoogle Scholar
34. Li D, Liu H, Zhang H, Wang X, Song F (2008) OsBIRH1, a DEAD-box RNA helicase with functions in modulating defence responses against pathogen infection and oxidative stress. J Exp Bot 59:2133–2146CrossRefPubMedPubMedCentralGoogle Scholar
35. Li Q, Chen LS, Jiang HX, Tang N, Yang LT, Lin ZH, Li Y, Yang GH (2010) Effects of manganese-excess on CO2 assimilation, ribulose-1, 5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. BMC Plant Biol 10:42CrossRefPubMedPubMedCentralGoogle Scholar
36. 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 15:615–628Google Scholar
37. Liang F, Cunningham KW, Harper JF, Sze H (1997) ECA1 complements yeast mutants defective in Ca2+ pumps and encodes an endoplasmic reticulum-type Ca2+-ATPase in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:8579–8584CrossRefPubMedPubMedCentralGoogle Scholar
38. Lionetti V, Raiola A, Camardella L, Giovane A, Obel N, Pauly M, Favaron F, Cervone F, Bellincampi D (2007) Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol 143:1871–1880CrossRefPubMedPubMedCentralGoogle Scholar
39. Liu S, Cao X, Liao Y, Chen R, Xu Z, Gao X, Lihua Li L, Zhu J (2015) Identification and characterization of a novel abiotic stress responsive ATPase gene from rice. Plant Omics J 8:169–177Google Scholar
40. Lu YB, Qi YP, Yang LT, Lee J, Guo P, Ye X, Jia MY, Li ML, Chen LS (2015) Long-term boron-deficiency-responsive genes revealed by cDNA-AFLP differ between Citrus sinensis roots and leaves. Front Plant Sci 6:585PubMedPubMedCentralGoogle Scholar
41. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13CrossRefGoogle Scholar
42. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
43. Marty P, Jouan B, Bertheau Y, Vian B, Goldberg R (1997) Charge density in stem cell walls of Solanum tuberosum genotypes and susceptibility to blackleg. Phytochemistry 44:1435–1441CrossRefGoogle Scholar
44. Mazau D, Esquerré-Tugayé MT (1986) Hydroxyproline-rich glycoprotein accumulation in the cell walls of plants infected by various pathogens. Physiol Mol Plant Pathol 29:147–157CrossRefGoogle Scholar
45. Mazzucotellin E, Mastrangelo AM, Crosatti C (2008) Abiotic stress response in plants: when post-transcriptional and posttranslational regulations control transcription. Plant Sci 174:420–431CrossRefGoogle Scholar
46. Mukhopadhyay MJ, Sharma A (1991) Manganese in cell metabolism of higher plants. Bot Rev 57(2):117–149CrossRefGoogle Scholar
47. Nakamura M, Yagi N, Kato T, Fujita S, Kawashima N, Ehrhardt DW, Hashimoto T (2012) Arabidopsis GCP3-interacting protein 1/MOZART 1 is an integral component of the γ-tubulin-containing microtubule nucleating complex. Plant J 71:216–225CrossRefPubMedGoogle Scholar
48. Negishi T, Oshima K, Hattori M, Kanai M, Mano S, Nishimura M, Yoshida K (2012) Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant. PLoS One 7:e43189CrossRefPubMedPubMedCentralGoogle Scholar
49. Pan H, Liu S, Tang D (2011) HPR1, a component of the THO/TREX complex, plays an important role in disease resistance and senescence in Arabidopsis. Plant J 69:831–843CrossRefPubMedGoogle Scholar
50. Papadakis IE, Giannakoula A, Therios IN, Bosabalidis AM, Moustakas M, Nastou A (2007) Mn-induced changes in leaf structure and chloroplast ultrastructure of Citrus volkameriana (L.) plants. J Plant Physiol 164:100–103CrossRefPubMedGoogle Scholar
51. Roy S (2014) Maintenance of genome stability in plants: repairing DNA double strand breaks and chromatin structure stability. Front Plant Sci 5:487CrossRefPubMedPubMedCentralGoogle Scholar
52. Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–442CrossRefGoogle Scholar
53. Seltzer V, Janski N, Canaday J, Herzog E, Erhardt M, Evrard JL, Schmit AC (2007) Arabidopsis GCP2 and GCP3 are part of a soluble γ-tubulin complex and have nuclear envelope targeting domains. Plant J 52:322–331CrossRefPubMedGoogle Scholar
54. Snider J, Thibault G, Houry WA (2008) The AAA+ superfamily of functionally diverse proteins. Genome Biol 9:216CrossRefPubMedPubMedCentralGoogle Scholar
55. Tan J, Tan Z, Wu F, Sheng P, Heng Y, Wang X, Ren Y, Wang J, Guo X, Zhang X, Cheng Z, Jiang L, Liu X, Wang H, Wan J (2014) A novel chloroplast-localized pentatricopeptide repeat protein involved in splicing affects chloroplast development and abiotic stress response in rice. Mol Plant 7:1329–1349CrossRefPubMedGoogle Scholar
56. Thapa G, Sadhukhan A, Panda SK, Sahoo L (2012) Molecular mechanistic model of plant heavy metal tolerance. Biometals 25:489–505CrossRefPubMedGoogle Scholar
57. Wang LQ, Yang LT, Guo P, Zhou XX, Ye X, Chen EJ, Chen LS (2015) Leaf cDNA-AFLP analysis reveals novel mechanisms for boron-induced alleviation of aluminum-toxicity in Citrus grandis seedlings. Ecotoxicol Environ Safe 120:349–359CrossRefGoogle Scholar
58. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB (2009) ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324:1076CrossRefPubMedPubMedCentralGoogle Scholar
59. Wu Z, Liang F, Hong B, Young JC, Sussman MR, Harper JF, Sze H (2002) An endoplasmic reticulum-bound Ca2+/Mn2+ pump, ECA1, supports plant growth and confers tolerance to Mn2+stress. Plant Physiol 130:128–137CrossRefPubMedPubMedCentralGoogle Scholar
60. Wu DM, Fu YQ, Yu ZW, Shen H (2013) Status of red soil acidification and aluminum toxicity in south China and prevention. Soils 45:577–584Google Scholar
61. Wu D, Ji J, Wang G, Guan C, Jin C (2014) LchERF, a novel ethylene-responsive transcription factor from Lycium chinense, confers salt tolerance in transgenic tobacco. Plant Cell Rep 33:2033–2045CrossRefPubMedGoogle Scholar
62. Xu X, Yang J, Zhao X, Zhang X, Li R (2015) Molecular binding mechanisms of manganese to the root cell wall of Phytolacca americana L. using multiple spectroscopic techniques. J Haz Mat 296:185–191CrossRefGoogle Scholar
63. Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611CrossRefPubMedPubMedCentralGoogle Scholar
64. Yang LT, Qi YP, Jiang HX, Chen LS (2013) Roles of organic acid anion secretion in aluminium tolerance of higher plants. BioMed Res Int 2013:173682PubMedGoogle Scholar
65. You X, Yang LT, Lu YB, Li H, Zhang SQ, Chen LS (2014) Proteomic changes of citrus roots in response to long-term manganese toxicity. Trees Struct Funct 28:1383–1399CrossRefGoogle Scholar
66. Zhao Y, Ma Q, Jin X, Peng X, Liu J, Deng L, Yan H, Sheng L, Jiang H, Cheng B (2014) A novel maize homeodomain-leucine zipper (HD-Zip) I gene, Zmhdz10, positively regulates drought and salt tolerance in both rice and Arabidopsis. Plant Cell Physiol 55:1142–1156CrossRefPubMedGoogle Scholar
67. Zhong H, Läuchli A (1993) Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. J Exp Bot 44:773–778CrossRefGoogle Scholar
68. Zhou CP, Qi YP, You X, Yang LT, Guo P, Ye X, Zhou XX, Ke FJ, Chen LS (2013) Leaf cDNA-AFLP analysis of two citrus species differing in manganese tolerance in response to long-term manganese-toxicity. BMC Genom 14:621CrossRefGoogle Scholar
69. Zhou XX, Yang LT, Qi YP, Guo P, Chen LS (2015) Mechanisms on boron-induced alleviation of aluminum-toxicity in Citrus grandis seedlings at a transcriptional level revealed by cDNA-AFLP analysis. PLoS One 10:e0115485CrossRefPubMedPubMedCentralGoogle Scholar
70. Zhu M, Li Y, Chen G, Ren L, Xie Q, Zhao Z, Hu Z (2015) Silencing SlELP2L, a tomato elongator complex protein 2-like gene, inhibits leaf growth, accelerates leaf, sepal senescence, and produces dark-green fruit. Sci Rep 5:7693CrossRefPubMedPubMedCentralGoogle Scholar

For further details log on website :
https://link.springer.com/article/10.1007%2Fs00468-016-1507-1