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Molecular Biology of Disease Resistance in Rice

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Molecular Biology of Disease Resistance in Rice Physiological and Molecular Plant Pathology (2001) 59, 1±11 doi:10.1006/pmpp.2001.0353, available online at http://www.idealibrary.com on MINI-REVIEW Molecular biology of disease resistance in rice FENGMING SONG1,2 and ROBERT M. GOODMAN1* 1Department of Plant Pathology, University of Wisconsin, 1630 Linden Drive, Madison, WI 53706, U.S.A. and 2Department of Plant Protection, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang, 310029, P.R. China (Accepted for publication 13 August 2001) Rice is one of the most important staple foods for the understanding the molecular biology of disease resistance increasing world population, especially in Asia. Diseases in rice is a prerequisite. are among the most important limiting factors that aect In recent years, rice has been recognized as a genetic rice production, causing annual yield loss conservatively model for molecular biology research aimed toward estimated at 5 %. More than 70 diseases caused by fungi, understanding mechanisms for growth, development and bacteria, viruses or nematodes have been recorded on rice stress tolerance as well as disease resistance [34]. Rice as a [68], among which rice blast (Magnaporthe grisea), model crop is a fortuitous situation since it is also a crop of bacterial leaf blight (Xanthomonas oryzae pv. oryzae) and world signi®cance. Rice is an attractive model for plant sheath blight (Rhizoctonia solani) are the most serious genetics and genomics because it has a relatively small constraints on high productivity [68]. Resistant cultivars genome. Considerable progress has been made in rice and application of pesticides have been used for disease towards cloning and identi®cation of disease resistance control. However, the useful life-span of many resistant genes, characterization of defense responses, and elucida- cultivars is only a few years, due to the breakdown of the tion of signal transduction leading to activation of defense resistance in the face of high pathogenic variability of the responses [93]. The results of this work provide new pathogen population. Use of pesticides is costly as well as insights into the molecular basis of disease resistance in environmentally undesirable. Thus, there is a need to rice. In this review, the focus is on the progress towards develop strategies providing durable resistance, giving the understanding of the molecular biology of disease protection for a long time and over a broad geographic resistance in rice against blast, bacterial leaf blight and area. Among such new strategies, systemic acquired sheath blight. resistance (SAR) is an example of a defense mechanism oering long-lasting disease resistance against a broad- spectrum of pathogens, and is promising for sustainable rice production in the future. New information and DISEASE RESISTANCE GENES IN RICE knowledge gained from research on the molecular biology of SAR as well as disease resistance gene-mediated The inheritance of resistance against blast and bacterial defense responses will undoubtedly provide new insights leaf blight diseases of rice has been extensively studied. into the nature of rice disease resistance, which in turn Major genes from various resistant donors have been oers opportunities for creating new rice varieties with identi®ed and to date more than 30 loci conditioning high resistance against multiple diseases. To this end, resistance against blast and 25 against bacterial leaf blight have been found [33, 43]. Some of these resistance * To whom all correspondence should be addressed. E-mail: genes or loci have been widely used in rice breeding [email protected] programs, and some of them have been mapped to their Abbreviations used in the text: AFLP, ampli®ed fragment length polymorphism; BTH, ben zothiadiazole; INA, dichlor- chromosomal locations and are subject to cloning eorts. oisonicotinic acid; LOX, lipoxygenase; LRD, leucine-rich To date, four resistance genes, Xa21 and Xa1 to bacterial domain; LRR, leucine rich repeats; MAP kinase, mitogen- leaf blight, and Pib and Pi-ta to blast, have been cloned activated protein kinase; PLD, Phospholipase D; PR, patho- and studied in detail at the molecular level [7, 86, 97, genesis-related; QTL, quantitative trait loci; RFLP, restriction 108]. Genetic variability for high levels of resistance fragment length polymorphism; RGA, resistance gene analogues; ROI, reactive oxygen intermediates; SA, salicylic against sheath blight is lacking in both cultivated rice and acid; SAR, systemic acquired resistance; Xoo, X.oryzae pv. its wild relatives [6]; therefore cloning of genes for sheath oryzae. blight resistance is lagging. 0885-5765/01/070001+11 $35.00/00 *c 2001 Academic Press 2 F. Song and R. M. Goodman Xa21 was transferred to the rice cultivar IR24 from the L6. The Xa1 protein contains two motifs of NBS in the wild species Oryza longistaminata and was found to confer amino-terminal half and an LRR domain in the resistance against many known X. oryzae pv. oryzae (Xoo) carboxyl-terminal half of the molecule. The LRR races in India and the Philippines [39]. Xa21 was cloned domain is composed of six almost perfect repeats, each by a map-based cloning strategy and found to encode a 93 amino acids long, with 62±99 % simple homology to receptor kinase-like protein carrying leucine-rich repeats each other at the amino acid level. Expression of Xa1 is (LRR) in the putative extracellular domain, a single induced upon wounding and infection by both compa- transmembrane domain and a serine/threonine kinase tible and incompatible strains of Xoo [108]. intracellular domain [86]. Compared with the proteins The dominant gene Pib confers high resistance to most encoded by other cloned plant disease-resistance genes, Japanese races of M. grisea, the causal agent of blast the structure of Xa21 protein is unique because it disease. Pib is located at the distal end of the long arm of contains the extracellular receptor LRR domain and chromosome 2. The Pib gene was cloned recently and the intracellular kinase domain. Xa21-mediated resistance found to encode a polypeptide of 1251 amino acids [97]. increases progressively from the susceptible juvenile two- The deduced protein encoded by Pib contains an NBS leaf stage through later stages, with 100 % resistance at region and C-terminal LRRs but no distinct transmem- the adult leaf 9/10 stage. Expression of Xa21 is inde- brane domain; thus, the Pib gene belongs to the NBS± pendent of plant developmental stage, infection with Xoo, LRR class of plant disease resistance genes. Interestingly, or wounding. These results suggest that Xa21-mediated the Pib protein contains an N-terminal duplication of the resistance is controlled by development either post- conserved kinase 1a (P-loop), 2 and 3a domains of NBS transcriptionally or by other factors [11]. Transgenic region and eight cysteine residues clustered in LRR 7 and rice plants expressing the cloned Xa21 showed the same 8. The signi®cance of the duplication and the clustered spectrum of resistance as did that of the donor line cysteine is unknown. Expression of Pib is induced by [88, 89, 93]. infection with both incompatible and compatible strains Xa21 is a member of a small multigene family of M. grisea and altered environmental conditions such as containing seven members; these members can be temperature and darkness [97]. grouped into two classes based on sequence similarity The Pi-ta gene sequence predicts a 928 amino acid [85]. The Xa21 class contains members Xa21, D and F; protein that is cytoplasmic and contains an NBS and a and class A2 contains A1, A2, C and E. The identity of leucine-rich carboxyl terminus [7]. The leucine-rich nucleotide sequence within each class is very high (98 % domain (LRD) in the predicted Pi-ta protein contains for Xa21 class and 95.2 % for A2 class), but only 63.5% an irregular highly imperfect repeating structure with the of the identity was observed between the two classes [85]. consensus LxxLxxL. Sequence analysis of 11 alleles of One member of the Xa21 family, Xa21D, encodes a Pi-ta from resistant, intermediate, and susceptible varie- receptor-like protein carrying LRR motifs in the pre- ties showed that the Pi-ta proteins in susceptible varieties sumed extracellular domain but lacks the transmembrane have one amino acid substitution compared with that in and cytoplasmic kinase domains [94]. In transgenic rice the resistant varieties. More than 40 % of the transgenic plants, Xa21D conferred partial resistance to Xoo at an plants biolistically transformed with the cloned Pi-ta gene intermediate level compared with that of Xa21 but or cDNA conferred resistance or intermediate resistance showed the same spectrum of resistance as Xa21. against blast, con®rming the identity of the cloned Pi-ta. However, other members (A1, A2, C, E and F) did not Interestingly, an R gene-like gene, RPR1, was cloned by confer any observable resistance in transgenic plants [94]. dierential display from probenazole-treated rice plants These results suggest that the extracellular LRR domain and was found to encode an NBS±LRR protein, sharing of Xa21D is involved in pathogen recognition. Moreover, structural similarity with the NBS±LRR class of R genes a highly conserved 233-bp sequence was identi®ed among [72]. RPR1 was mapped to a region close to the location of all seven Xa21 family members [85] and 15 transposon- Pi-ta on chromosome 11. These features suggested that like elements were found within the gene cluster [84], RPR1 might act as a resistance gene. The expression suggesting that these elements may play a role in the of RPR1 in rice can be induced by both treatments with diversi®cation of the Xa21 family members, probably by SAR inducers such as salicylic acid (SA) or benzothia- duplication, recombination and transposition. diazole (BTH) and by infection with M. grisea. Xa1 confers a high level of speci®c resistance to race 1 In addition to these cloned disease resistance genes strains of Xoo in Japan.
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