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Journal of Integrative Agriculture  2018, Vol. 17 Issue (09): 1946-1958    DOI: 10.1016/S2095-3119(17)61832-X
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Transcriptomic responses to aluminum (Al) stress in maize
XU Li-ming1, LIU Chan1, CUI Bao-ming2, WANG Ning1, ZHAO Zhuo1, ZHOU Li-na1, HUANG Kai-feng1, DING Jian-zhou1, DU Han-mei1, JIANG Wei1, ZHANG Su-zhi1
1 Key Laboratory of Biology and Genetic Improvement of Maize in Southwest China, Ministry of Agriculture/Maize Research Institute, Sichuan Agricultural University, Chengdu 611130, P.R.China
2 Crop Research Institute of Binzhou, Binzhou 256600, P.R.China
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Aluminum (Al) toxicity is a major factor limiting crop production and plant growth in acid soils.  The complex inheritance of Al toxicity and tolerance mechanisms in maize has uncharacterized yet.  In this study, the maize inbred line 178 seedlings were treated with 200 μmol L–1 CaCl2+0 μmol L–1 AlCl3 (control) and 200 μmol L–1 CaCl2+60 μmol L–1 AlCl3 (Al treatment) for 1 and 6 h, respectively.  The experiment was repeated three times.  Then a detailed temporal analysis of root gene expression was performed using an Agilent GeneChip with 34 715 genes, only the genes showing more than 2.0-fold difference (P<0.01) between the control and the Al treatment maize seedlings were analyzed further.  Thus, a total of 832 different expression genes, 689 significantly up-regulated and 143 down-regulated, were identified after the seedlings were treated with Al for 6 h.  And 60 genes, 59 up-regulated and one down-regulated, were also detected after the seedlings were treated for 1 h.  Replicated transcriptome analyses further showed that about 61% of total significantly genes could be annotated based on plant genome resources.  Quantitative real-time PCR (qRT-PCT) of some selected candidate genes was used to demonstrate the microarray data, indicating significant differences between the control and Al-treated seedlings.  Exposure to Al for 6 h triggered changes in the transcript levels for several genes, which were primarily related to cell wall structure and metabolism, oxidative stress response, membrane transporters, organic acid metabolism, signaling and hormones, and transcription factors, etc.  After Al-treated for 1 h, differential abundance of transcripts for several transporters, kinase, and transcription factors were specifically induced.  In this study, the diversity of the putative functions of these genes indicates that Al stress for a short stage induced a complex transcriptome changes in maize.  These results would further help us to understand rapid and early mechanisms of Al toxicity and tolerance in maize regulated at the transcriptional level.
Keywords:  aluminum        maize        microarray        mechanism        transcriptome  
Received: 27 September 2017   Accepted: 14 August 2018
Fund: This work was supported by the National Basic Research Program of China (973 Program, 2014CB138705) and the National Natural Science Foundation of China (30800687, 31071434), and the Ph D Programs Foundation of Ministry of Education of China (1.20125103110011).
Corresponding Authors:  Correspondence ZHANG Su-zhi, Tel/Fax: +86-28-86290916, E-mail:   

Cite this article: 

XU Li-ming, LIU Chan, CUI Bao-ming, WANG Ning, ZHAO Zhuo, ZHOU Li-na, HUANG Kai-feng, DING Jian-zhou, DU Han-mei, JIANG Wei, ZHANG Su-zhi. 2018. Transcriptomic responses to aluminum (Al) stress in maize. Journal of Integrative Agriculture, 17(09): 1946-1958.

Basu U, Taylor G J. 1994. Differential exudation of polypeptides by roots of aluminum-resistant and aluminum-sensitive cultivars of Triticum aestivum L. in response to aluminum stress.  Plant Physiology, 106, 151–158.
Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annual Review of Plant Biology, 54, 519–546.
Chandran D, Sharopova N, Ivashuta S, Gantt J S, Vandenbosch K A, Samac D A. 2008. Transcriptome profiling identified novel genes associated with aluminum toxicity, resistance and tolerance in Medicago truncatula. Planta, 228, 151–166.
Cheng N. 2008. AtGRX4, an Arabidopsis chloroplastic monothiol glutaredoxin, is able to suppress yeast grx5 mutant phenotypes and respond to oxidative stress. FEBS Letters, 582, 848–854.
Cheng N H, Liu J Z, Brock A, Nelson R S. 2006. AtGRXcp, an Arabidopsis chloroplastic glutaredoxin, is critical for protection against protein oxidative damage. Journal of Biological Chemistry, 281, 26280–26288.
Debeaujon I, Peeters A J M, Léonkloosterziel K M, Koornneef M. 2001. The transparent testa12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. The Plant Cell, 13, 853–871.
Degenhardt J, Larsen P B, Howell S H , Kochian L V. 1998. Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH. Plant Physiology, 117, 19–27.
Delhaize E, Ryan P R. 1995. Aluminum toxicity and tolerance in plants. Plant Physiology, 107, 315–321.
Delhaize E, Ryan P R, Randall P J. 1993. Aluminum tolerance in wheat (Triticum aestivum L.). II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiology, 103, 695–702.
Diener A C, Gaxiola R A, Fink G R. 2001. Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. The Plant Cell, 13, 1625–1637.
Dixon R A, Achnine L, Kota P, Liu C J, Reddy M S, Wang L. 2002. The phenylpropanoid pathway and plant defence - A genomics perspective. Molecular Plant Pathology, 3, 371–390.
Duressa D, Soliman K M, Taylor R W, Chen D. 2011. Gene expression profiling in soybean under aluminum stress: Genes differentially expressed between Al-tolerant and Al-sensitive genotypes. American Journal of Molecular Biology, 1, 156–173.
Emmanuel D, Gruber B D, Ryan P R. 2007. The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Letters, 581, 2255–2262.
Eticha D, Zahn M, Bremer M, Yang Z, Rangel A F, Rao I M, Horst W J. 2010. Transcriptomic analysis reveals differential gene expression in response to aluminium in common bean (Phaseolus vulgaris) genotypes. Annals of Botany, 105, 1119–1128.
Ezaki B, Katsuhara M, Kawamura M, Matsumoto H. 2001. Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiology, 127, 918–927.
Frantzios G, Galatis B, Apostolakos P. 2001. Aluminium effects on microtubule organization in dividing root-tip cells of Triticum turgidum. II. Cytokinetic cells. Journal of Plant Research, 114, 157–170.
Furukawa J, Yamaji N, Hua W, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Jian F M. 2007. An aluminum-activated citrate transporter in barley. Plant & Cell Physiology, 48, 1081–1091.
Guo P, Bai G, Carver B, Li R, Bernardo A, Baum M. 2007. Transcriptional analysis between two wheat near-isogenic lines contrasting in aluminum tolerance under aluminum stress. Molecular Genetics & Genomics, 277, 1–12.
Hayes J E, Ma J F. 2003. Al-induced efflux of organic acid anions is poorly associated with internal organic acid metabolism in triticale roots. Journal of Experimental Botany, 54, 1753–1759.
Herrmann K M, Weaver L M. 1999. The shikimate pathway. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 473–503.
Horst W J, Kollmeier M, Schmohl N, Sivaguru M, Wang Y, Felle H H, Hedrich R, Schröder W, Staß A. 2007. Significance of the root apoplast for aluminium toxicity and resistance of maize. In: Sattelmacher B, Horst W J, eds., The Apoplast of Higher Plants: Compartment of Storage, Transport and Reactions. Springer Netherlands, Germany. pp. 49–66.
Horst W J, Wang Y, Eticha D. 2010. The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: A review. Annals of Botany, 106, 185–197.
Iwata Y, Fedoroff N V, Koizumi N. 2008. Arabidopsis bzip60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. The Plant Cell, 20, 3107–3121.
Jan A, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K. 2013. Ostzf1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiology, 161, 1202–1216.
Jorge R A, Arruda P. 1997. Aluminum-induced organic acids exudation by roots of an aluminum-tolerant tropical maize. Phytochemistry, 45, 675–681.
Kaczorek T, Rogowski K. 2002. A gene encoding multidrug resistance (mdr)-like protein is induced by aluminum and inhibitors of calcium flux in wheat. Plant & Cell Physiology, 43, 177–185.
Knaggs, Andrew R. 2003. The biosynthesis of shikimate metabolites. Natural Product Reports, 20, 119–136.
Kobayashi Y, Hoekenga O A, Itoh H, Nakashima M, Saito S, Shaff J E, Maron L G, Piñeros M A, Kochian L V, Koyama H. 2007. Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiology, 145, 843–852.
Kochian L V. 2003. Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Biology, 46, 237–260.
Kochian L V, Hoekenga O A, Pi M A. 2004. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annual Review of Plant Biology, 55, 459–493.
Kochian L V, Piñeros M A, Hoekenga O A. 2005. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant & Soil, 274, 175–195.
Kollmeier M, Felle H H, Horst W J. 2000. Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiology, 122, 945–956.
Koshiba T, Saito E, Ono N, Yamamoto N, Sato M. 1996. Purification and properties of flavin- and molybdenum-containing aldehyde oxidase from coleoptiles of maize. Plant Physiology, 110, 781–789.
Kumari M, Taylor G J, Deyholos M K. 2008. Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. Molecular Genetics & Genomics, 279, 339–357.
Kusano T, Berberich T, Harada M, Suzuki N, Sugawara K. 1995. A maize DNA-binding factor with a bZIP motif is induced by low temperature. Molecular & General Genetics, 248, 507–517.
Li X F, Matsumoto H. 2000. Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiology, 123, 1537–1543.
Lorenc K, Korobczak A, Aksamit S A, Kostyń K, Lukaszewicz M, Szopa J. 2004. Glucosyltransferase: The gene arrangement and enzyme function. Cellular & Molecular Biology Letters, 9, 935–946.
Lyza G M, Matias K, Chuanzao M, Matthew J M, Marcelo M, Leon V K. 2008. Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytologist, 179, 116–128.
Ma J F, Hiradate S. 2000. Form of aluminium for uptake and translocation in buckwheat (Fagopyrum esculentum Moench). Planta, 211, 355–360.
Mattiello L, Kirst M, da Silva F R, Jorge R A, Menossi M. 2010. Transcriptional profile of maize roots under acid soil growth. BMC Plant Biology, 10, 196–196.
Meyer Y, Belin C, Delormehinoux V, Reichheld J P, Riondet C. 2012. Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxidants & Redox Signaling, 17, 1124–1160.
Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405–410.
Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2012. NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta-General Subjects, 1819, 97–103.
Oono Y, Wakasa Y, Hirose S, Yang L, Sakuta C, Takaiwa F. 2010. Analysis of ER stress in developing rice endosperm accumulating beta-amyloid peptide. Plant Biotechnology Journal, 8, 691–718.
Osawa H, Matsumoto H. 2001. Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex. Plant Physiology, 126, 411–420.
Pedersen L C, Jian D, Fumiyasu T, Hiroshi K, Krahn J M, Pedersen L G, Kazuyuki S, Masahiko N. 2003. Crystal structure of an alpha 1,4-N-acetylhexosaminyltransferase (EXTL2), a member of the exostosin gene family involved in heparan sulfate biosynthesis. Journal of Biological Chemistry, 278, 14420–14428.
Piñeros M A, Maron L G, Guimarães C T, Magalhaes J V, Pleiman J K, Mao C, Shaff J, Belicuas S N J, Kochian L V. 2010. Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. The Plant Journal, 61, 728–740.
Qin L X, Li Y, Li D D, Xu W L, Zheng Y, Li X B. 2014. Arabidopsis drought-induced protein Di19-3 participates in plant response to drought and high salinity stresses. Plant Molecular Biology, 86, 609–625.
Rodriguez P L. 1998. Protein phosphatase 2C (PP2C) function in higher plants. Plant Molecular Biology, 38, 919–927.
Ryan P R, Delhaize E, Jones D L. 2001. Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology & Plant Molecular Biology, 52, 527-560.
Sang G K, Yong H C, Lee J S, Schlesinger S R, Zabet-Moghaddam M, Chung J S, Knaff D B, Sun T K, Sang Y L, Kim S K. 2010. Redox properties of a thioredoxin-like Arabidopsis protein, AtTDX. Biochimica et Biophysica Acta, 1804, 2213–2221.
Sasaki M, Yamamoto Y, Matsumoto H. 1996. Lignin deposition induced by aluminum in wheat (Triticum aestivum) roots. Physiologia Plantarum, 96, 193–198.
Schmohl N J, Fisahn J, Horst W J. 2000. Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiologia Plantarum, 109, 419–427.
Shen H, Ligaba A, Yamaguchi M, Osawa H, Shibata K, Yan X, Matsumoto H. 2004. Effect of K‐252a and abscisic acid on the efflux of citrate from soybean roots. Journal of Experimental Botany, 55, 663–671.
Singh S K, Eland C, Harholt J, Scheller H V, Marchant A. 2005. Cell adhesion in Arabidopsis thaliana is mediated by ECTOPICALLY PARTING CELLS 1 - A glycosyltransferase (GT64) related to the animal exostosins.  The Plant Journal, 43, 384–397.
Sivaguru M, Ezaki B, He Z H, Tong H, Osawa H, Baluška F, Volkmann D, Matsumoto H. 2003. Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiology, 132, 2256–2266.
Sivaguru M, Horst W J. 1998. The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiology, 116, 155–163.
Taylor G J, Mcdonald-Stephens J L, Hunter D B, Bertsch P M, Elmore D, Rengel Z, Reid R J. 2000. Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiology, 123, 987–996.
Tesfaye M, Temple S J, Allan D L, Vance C P, Samac D A. 2001. Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiology, 127, 1836–1844.
Vercauteren I, De A E, De G R, Gheysen G. 2002. An Arabidopsis thaliana pectin acetylesterase gene is up-regulated in nematode feeding sites induced by root-knot and cyst nematodes. Molecular Plant-Microbe Interactions, 15, 404–407.
Vij S, Tyagi A K. 2007. Emerging trends in the functional genomics of the abiotic stress response in crop plants. Plant Biotechnology Journal, 5, 361–380.
Wang K L, Yoshida H, Lurin C, Ecker J R. 2004. Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature, 428, 945–950.
Wen F, Zhu Y, Hawes M C. 1999. Effect of pectin methylesterase gene expression on pea root development. The Plant Cell, 11, 1129–1140.
Wera S, Hemmings B A. 1995. Serine/threonine protein phosphatases. Biochemical Journal, 311, 17–29.
Xu Y, Niu X L, Yang S H, LI Y X, Liu L L, Tang W, Liu Y S. 2011. Research on heat and drought tolerance in rice (Oryza sativa) by overexpressing transcription factor osbzip60. Scientia Agricultura Sinica, 44, 4142–4149. (in Chinese)
Yamamoto Y, Kobayashi Y, Devi S R, Rikiishi S, Matsumoto H. 2002. Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiology, 128, 63–72.
Yang J L, Li Y Y, Zhang Y J, Zhang S S, Wu Y R, Wu P, Zheng S J. 2008. Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiology, 146, 602–611.
Yang Y, Cheng J Z, Singhal S S, Saini M, Pandya U, Awasthi S, Awasthi Y C. 2001. Role of glutathione S-transferases in protection against lipid peroxidation. Overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation. Journal of Biological Chemistry, 276, 19220–19230.
Yoshida H, Nagata M, Saito K, Wang K L, Ecker J R. 2005. Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 I-aminocyclopropane-I-carboxylate synthases. BMC Plant Biology, 5, 216–220.
You J F, Zhang H M, Liu N, Gao L L, Kong L N, Yang Z M. 2011. Transcriptomic responses to aluminum stress in soybean roots. Genome, 54, 923–933.
Zg E, Zhang Y P, Zhou J H, Wang L. 2014. Mini review: Roles of the bZIP gene family in rice. Genetics & Molecular Research, 13, 3025–3036.
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