A unique aluminum resistance mechanism conferred by aluminum and salicylic-acid-activated root efflux of benzoxazinoids in maize
- 343 Downloads
Background and aims
Although aluminum (Al) exclusion via root exudation of organic matters is a common resistance mechanism adopted by many plant species, whether root exudation of benzoxazinoids, such as hydroxamic acids (HAs), confers Al resistance remains unclear.
We performed physiological characterization for an Al-resistant maize cultivar TY and a sensitive maize cultivar ZD.
First, Al exposure induced HA exudation from the root tip of TY, but not from ZD. Second, HAs formed non-toxic Al chelation complexes in vitro and exogenous HAs alleviated root damage and improved root growth under Al stresses. Third, both Al and exogenous salicylic acid (SA) treatments induced accumulation of endogenous SAs in the root apices of TY, which in turn enhanced root HA exudation and Al resistance in TY. Furthermore, an SA biosynthesis inhibitor significantly decreased Al resistance in TY and abolished the beneficial effects of exogenous SA on Al resistance, suggesting a key role of the endogenous SAs in induction of Al resistance. Finally, it was the root-tip HA exudation but not the root-tip HA contents that determined Al resistance in maize.
We have revealed a unique Al exclusion mechanism underlying Al resistance via Al and SA-mediated root HA efflux in maize.
KeywordsAluminum tolerance Benxozaxinoids Hydroxamic acids Maize Root exudate Salicylic acid
This study is supported by the National Natural Science Foundation of China (grant NO. 31201680) and Guangxi Natural Science Foundation (grant NO. 2012GXNSFAA053047 and NO. 2016GXNSFAA380230).
This study was conceived and supervised by XL, MG, ZZ, JL and XT; XG, YK, MC and LX performed the experiments. The manuscript was written by ZZ, XT and JL and was reviewed by all authors.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Bakera B, Makowska B, Groszyk J, Niziołek M, Orczyk W, Bolibok-Brągoszewska H, Hromada-Judycka A, Rakoczy-Trojanowska M (2015) Structural characteristics of ScBx genes controlling the biosynthesis of hydroxamic acids in rye (Secale cereale L.). J Appl Genet 56:287–298. https://doi.org/10.1007/s13353-015-0271-z CrossRefPubMedPubMedCentralGoogle Scholar
- Chen K-J, Zheng Y-Q, Kong C-H, Zhang S-Z, Li J, Liu X-G (2010) 2, 4-Dihydroxy-7-methoxy-1, 4-benzoxazin-3-one (DIMBOA) and 6-methoxy-benzoxazolin-2-one (MBOA) levels in the wheat rhizosphere and their effect on the soil microbial community structure. J Agric Food Chem 58:12710–12716. https://doi.org/10.1021/jf1032608 CrossRefPubMedGoogle Scholar
- Grün S, Frey M, Gierl A (2005) Evolution of the indole alkaloid biosynthesis in the genus Hordeum: distribution of gramine and DIBOA and isolation of the benzoxazinoid biosynthesis genes from Hordeum lechleri. Phytochem 66:1264–1272. https://doi.org/10.1016/j.phytochem.2005.01.024 CrossRefGoogle Scholar
- Guimaraes CT, Simoes CC, Pastina MM, Maron LG, Magalhaes JV, Vasconcellos RC, Guimaraes LJ, Lana UG, Tinoco CF, Noda RW, Jardim-Belicuas SN, Kochian LV, Alves VMC, Parentoni S (2014) Genetic dissection of Al tolerance QTLs in the maize genome by high density SNP scan. BMC Genomics 15:153. https://doi.org/10.1186/1471-2164-15-153 CrossRefPubMedPubMedCentralGoogle Scholar
- Kidd P, Llugany M, Poschenrieder C, Gunse B, Barcelo J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52:1339–1352. https://doi.org/10.1093/jxb/52.359.1339 CrossRefPubMedGoogle Scholar
- Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493. https://doi.org/10.1146/annurev.arplant.55.031903.141655 CrossRefPubMedGoogle Scholar
- Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598. https://doi.org/10.1146/annurev-arplant-043014-114822 CrossRefPubMedGoogle Scholar
- Leszczynski B, Dixon AF (1990) Resistance of cereals to aphids: interaction between hydroxamic acids and the aphid Sitobion avenae (Homoptera: Aphididae). Ann Appl Biol 117:21–30. https://doi.org/10.1111/j.1744-7348.1990.tb04191.x CrossRefGoogle Scholar
- Li XF, Ma JF, Hiradate S, Matsumoto H (2000) Mucilage strongly binds aluminum but does not prevent roots from aluminum injury in Zea mays. Physiol Plant 108:152–160. https://doi.org/10.1034/j.1399-3054.2000.108002152.x CrossRefGoogle Scholar
- Liang C, Piñeros M, Tian J, Yao Z, Sun L, Liu J, Shaff J, Coluccio A, Kochian L, Liao H (2013) Low pH, aluminum and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol 161:1347–1361. https://doi.org/10.1104/pp.112.208934 CrossRefPubMedPubMedCentralGoogle Scholar
- Liu J, Luo X, Shaff J, Liang C, Jia X, Li Z, Magalhaes J, Kochian LV (2012a) A promoter-swap strategy between the AtALMT and AtMATE genes increased Arabidopsis aluminum resistance and improved carbon-use efficiency for aluminum resistance. Plant J 71:327–337. https://doi.org/10.1111/j.1365-313X.2012.04994.x CrossRefPubMedGoogle Scholar
- Lu C, Liu X, Xu J, Dong F, Zhang C, Tian Y, Zheng Y (2012) Enhanced exudation of DIMBOA and MBOA by wheat seedlings alone and in proximity to wild oat (Avena fatua) and flixweed (Descurainia sophia). Weed Sci 60:360–365. https://doi.org/10.1614/WS-D-l1-00119.1.
- Ma JF (2005) Physiological mechanisms of Al resistance in higher plants. Soil Sci Plant Nutr 51:609–612. https://doi.org/10.1111/j.1747-0765.2005.tb00074.x CrossRefGoogle Scholar
- Magalhaes JV, Liu J, Guimaraes CT, Lana UG, Alves VM, Wang Y-H, Schaffert RE, Hoekenga OA, Pineros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161. https://doi.org/10.1038/ng2074 CrossRefPubMedGoogle Scholar
- Makleit P (2005) Changes in cyclic hydroxamic acid content of various rye varieties for the effect of abiotic stress. Acta Biol Szeged 49:103–104 http://abs.bibl.u-szeged.hu/index.php/abs/article/view/2435 Google Scholar
- Melo JO, Lana UG, Piñeros MA, Alves VM, Guimarães CT, Liu J, Zheng Y, Zhong S, Fei Z, Maron LG, Schaffert RE, Kochian LV (2013) Incomplete transfer of accessory loci influencing SbMATE expression underlies genetic background effects for aluminum tolerance in sorghum. Plant J 73:276–288. https://doi.org/10.1111/tpj.12029 CrossRefPubMedGoogle Scholar
- Niemeyer HM, Perez FJ (1995) Potential of hydroxamic acids in the control of cereal pests, diseases, and weeds. In: Allelopathy: Organisms, Processes and Applications.Google Scholar
- Pandey P, Srivastava RK, Dubey R (2013) Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. Ecotoxicology 22:656–670. https://doi.org/10.1007/s10646-013-1058-9 CrossRefPubMedGoogle Scholar
- Raskin I, Skubatz H, Tang W, Meeuse BJ (1990) Salicylic acid levels in thermogenic and non-thermogenic plants. Ann Bot 66:369–373. https://doi.org/10.1093/oxfordjournals.aob.a088037 CrossRefGoogle Scholar
- Song YY, Cao M, Xie LJ, Liang XT, Zeng RS, Su YJ, Huang JH, Wang RL, Luo SM (2011) Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight. Mycorrhiza 21:721–731. https://doi.org/10.1007/s00572-011-0380-4 CrossRefPubMedGoogle Scholar
- Tang X, Guo T, Gao X, Li XF, Gu M (2015) The Relationship between Hydroxamates Cyclic Secretion from Maize and Its Tolerance to Aluminum. Ecol Environ Sci 24:547–553. https://doi.org/10.16258/j.cnki.1674-5906.2015.04.001 CrossRefGoogle Scholar
- Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206. https://doi.org/10.1146/annurev.phyto.050908.135202 CrossRefPubMedPubMedCentralGoogle Scholar
- Wang Y, Li R, Li D, Jia X, Zhou D, Li J, Lyi SM, Hou S, Huang Y, Kochian LV, Liu J (2017) NIP1; 2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis. Proc Natl Acad Sci U S A 114:5047–5052. https://doi.org/10.1073/pnas.1618557114 CrossRefPubMedPubMedCentralGoogle Scholar
- Wouters FC, Gershenzon J, Vassão DG (2016) Benzoxazinoids: reactivity and modes of action of a versatile class of plant chemical defenses. J Brazil Chem Soc 27: 1379–1397. https://doi.org/10.5935/0103-5053.20160177.