Benzoxazinoid Metabolites Regulate Innate Immunity against Aphids and Fungi in Maize

被引:271
作者
Ahmad, Shakoor [1 ,6 ]
Veyrat, Nathalie [1 ,2 ]
Gordon-Weeks, Ruth [1 ]
Zhang, Yuhua [1 ]
Martin, Janet [1 ]
Smart, Lesley [1 ]
Glauser, Gaetan [2 ,3 ]
Erb, Matthias [2 ]
Flors, Victor [4 ]
Frey, Monika [5 ]
Ton, Jurriaan [1 ,7 ]
机构
[1] Ctr Sustainable Pest & Dis Management, Harpenden AL5 4JQ, Herts, England
[2] Univ Neuchatel, Lab Fundamental & Appl Res Chem Ecol, CH-2009 Neuchatel, Switzerland
[3] Univ Neuchatel, Chem Analyt Serv Swiss Plant Sci Web, CH-2009 Neuchatel, Switzerland
[4] Univ Jaume 1, Dept Expt Sci, Plant Physiol Sect, Castellon de La Plana 12071, Spain
[5] Tech Univ Munich, D-85354 Freising Weihenstephan, Germany
[6] Univ Utrecht, Fac Sci, Inst Environm Biol, NL-3508 TB Utrecht, Netherlands
[7] Univ Sheffield, Dept Anim & Plant Sci, Sheffield S10 2TN, S Yorkshire, England
基金
英国生物技术与生命科学研究理事会;
关键词
HYDROXAMIC ACIDS; ARABIDOPSIS-THALIANA; ABSCISIC-ACID; INDUCED RESISTANCE; BETA-GLUCOSIDASES; DEFENSE CHEMICALS; HDMBOA-GLC; PCR DATA; GENE; INDOLE;
D O I
10.1104/pp.111.180224
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Benzoxazinoids (BXs), such as 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), are secondary metabolites in grasses. The first step in BX biosynthesis converts indole-3-glycerol phosphate into indole. In maize (Zea mays), this reaction is catalyzed by either BENZOXAZINELESS1 (BX1) or INDOLE GLYCEROL PHOSPHATE LYASE (IGL). The Bx1 gene is under developmental control and is mainly responsible for BX production, whereas the Igl gene is inducible by stress signals, such as wounding, herbivory, or jasmonates. To determine the role of BXs in defense against aphids and fungi, we compared basal resistance between Bx1 wild-type and bx1 mutant lines in the igl mutant background, thereby preventing BX production from IGL. Compared to Bx1 wild-type plants, BX-deficient bx1 mutant plants allowed better development of the cereal aphid Rhopalosiphum padi, and were affected in penetration resistance against the fungus Setosphaeria turtica. At stages preceding major tissue disruption, R. padi and S. turtica elicited increased accumulation of DIMBOA-glucoside, DIMBOA, and 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one-glucoside (HDMBOA-glc), which was most pronounced in apoplastic leaf extracts. Treatment with the defense elicitor chitosan similarly enhanced apoplastic accumulation of DIMBOA and HDMBOA-glc, but repressed transcription of genes controlling BX biosynthesis downstream of BX1. This repression was also obtained after treatment with the BX precursor indole and DIMBOA, but not with HDMBOA-glc. Furthermore, BX-deficient bx1 mutant lines deposited less chitosan-induced callose than Bx1 wild-type lines, whereas apoplast infiltration with DIMBOA, but not HDMBOA-glc, mimicked chitosan-induced callose. Hence, DIMBOA functions as a defense regulatory signal in maize innate immunity, which acts in addition to its well-characterized activity as a biocidal defense metabolite.
引用
收藏
页码:317 / 327
页数:11
相关论文
共 55 条
[1]  
Agrios G.N., 1997, Plant Pathology, VFourth
[2]   Genetic dissection of basal defence responsiveness in accessions of Arabidopsis thaliana [J].
Ahmad, Shakoor ;
Van Hulten, Marieke ;
Martin, Janet ;
Pieterse, Corne M. J. ;
Van Wees, Saskia C. M. ;
Ton, Jurriaan .
PLANT CELL AND ENVIRONMENT, 2011, 34 (07) :1191-1206
[3]   ROLE OF HYDROXAMIC ACIDS IN THE RESISTANCE OF CEREALS TO APHIDS [J].
ARGANDONA, VH ;
LUZA, JG ;
NIEMEYER, HM ;
CORCUERA, LJ .
PHYTOCHEMISTRY, 1980, 19 (08) :1665-1668
[4]   MAIZE MICROSOMAL BENZOXAZINONE N-MONOOXYGENASE [J].
BAILEY, BA ;
LARSON, RL .
PLANT PHYSIOLOGY, 1991, 95 (03) :792-796
[5]   Benzoxazinoids-cyclic hydroxamic acids, lactams and their corresponding glucosides in the genus Aphelandra (Acanthaceae) [J].
Baumeler, A ;
Hesse, M ;
Werner, C .
PHYTOCHEMISTRY, 2000, 53 (02) :213-222
[6]   A Glucosinolate Metabolism Pathway in Living Plant Cells Mediates Broad-Spectrum Antifungal Defense [J].
Bednarek, Pawel ;
Pislewska-Bednarek, Mariola ;
Svatos, Ales ;
Schneider, Bernd ;
Doubsky, Jan ;
Mansurova, Madina ;
Humphry, Matt ;
Consonni, Chiara ;
Panstruga, Ralph ;
Sanchez-Vallet, Andrea ;
Molina, Antonio ;
Schulze-Lefert, Paul .
SCIENCE, 2009, 323 (5910) :101-106
[7]   CLONING AND CHARACTERIZATION OF THE MAIZE AN1 GENE [J].
BENSEN, RJ ;
JOHAL, GS ;
CRANE, VC ;
TOSSBERG, JT ;
SCHNABLE, PS ;
MEELEY, RB ;
BRIGGS, SP .
PLANT CELL, 1995, 7 (01) :75-84
[8]   Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes:: Identification by mass spectrometry and bioinformatics [J].
Boudart, G ;
Jamet, E ;
Rossignol, M ;
Lafitte, C ;
Borderies, G ;
Jauneau, A ;
Esquerré-Tugayé, MT ;
Pont-Lezica, R .
PROTEOMICS, 2005, 5 (01) :212-221
[9]   Effects of 1,4-benzoxazin-3-one derivatives from maize on survival and fecundity of Metopolophium dirhodum (Walker) on artificial diet [J].
Cambier, V ;
Hance, T ;
De Hoffmann, E .
JOURNAL OF CHEMICAL ECOLOGY, 2001, 27 (02) :359-370
[10]   Resistance loci affecting distinct stages of fungal pathogenesis: use of introgression lines for QTL mapping and characterization in the maize - Setosphaeria turcica pathosystem [J].
Chung, Chia-Lin ;
Longfellow, Joy M. ;
Walsh, Ellie K. ;
Kerdieh, Zura ;
Van Esbroeck, George ;
Balint-Kurti, Peter ;
Nelson, Rebecca J. .
BMC PLANT BIOLOGY, 2010, 10