Identification of a Novel Semi-Dominant Spotted-Leaf Mutant with Enhanced Resistance to Xanthomonas oryzae pv. oryzae in Rice
Abstract
:1. Introduction
2. Results
2.1. Performance of Agronomic Traits
2.2. Impaired Function of Photosynthetic Capacity
2.3. Lesion Initiation Is Light-Dependent
2.4. ROS-Associated Cell Death Occurs in spl24
2.5. Enhanced Disease Resistance to Xoo with Elevated Expression of Defense Response Genes
2.6. SPL24-Mediated Disease Resistance Is Associated With the Activation of SA Signaling Pathway
2.7. Genetic Control and Physical Mapping of OsSPL24
3. Discussion
4. Materials and Methods
4.1. Plant Materials and Growth Conditions
4.2. Senescence-related Parameter Measurement
4.3. Shading Experiment
4.4. Histochemical Analysis
4.5. TUNEL Experiment
4.6. RNA Extraction and qRT-PCR
4.7. Disease Evaluation and Phytohormone Level Determination
4.8. Genetic Analysis and Gene Mapping
4.9. Transcriptome Analysis
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Huang, Q.N.; Yang, Y.; Shi, Y.F.; Wu, J.L. Spotted-leaf mutants of rice (Oryza sativa). Rice Sci. 2010, 17, 247–256. [Google Scholar] [CrossRef]
- Feng, B.H.; Yang, Y.; Shi, Y.F.; Shen, H.C.; Wang, H.M.; Huang, Q.N.; Xu, X.; Lü, X.G.; Wu, J.L. Characterization and genetic analysis of a novel rice spotted-leaf mutant HM47 with broad-spectrum resistance to Xanthomonas oryzae pv. oryzae. J. Integr. Plant Biol. 2013, 55, 473–483. [Google Scholar] [CrossRef] [PubMed]
- Huang, Q.N.; Shi, Y.F.; Yang, Y.; Feng, B.H.; Wei, Y.L.; Chen, J.; Baraoidan, M.; Leung, H.; Wu, J.L. Characterization and genetic analysis of a light-and temperature-sensitive spotted-leaf mutant in rice. J. Integr. Plant Biol. 2011, 53, 671–681. [Google Scholar] [CrossRef] [PubMed]
- Shen, H.C.; Shi, Y.F.; Feng, B.H.; Wang, H.M.; Xu, X.; Huang, Q.N.; Lü, X.G.; Wu, J.L. Identification and genetic analysis of a novel rice spotted-leaf mutant with broad-spectrum resistance to Xanthomonas oryzae, pv. oryzae. J. Integr. Agric. 2014, 13, 713–721. [Google Scholar] [CrossRef]
- Huang, Q.N.; Shi, Y.F.; Zhang, X.B.; Song, L.X.; Feng, B.H.; Wang, H.M.; Xu, X.; Li, X.H.; Guo, D.; Wu, J.L. Single base substitution in OsCDC48 is responsible for premature senescence and death phenotype in rice. J. Integr. Plant Biol. 2016, 58, 12–28. [Google Scholar] [CrossRef] [PubMed]
- Yamanouchi, U.; Yano, M.; Lin, H.; Ashikari, M.; Yamada, K. A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc. Natl. Acad. Sci. USA. 2002, 99, 7530–7535. [Google Scholar] [CrossRef] [PubMed]
- Zeng, L.R.; Qu, S.; Bordeos, A.; Yang, C.; Baraoidan, M.; Yan, H.; Xie, Q.; Nahm, B.H.; Leung, H.; Wang, G.L. Spotted leaf 11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 2004, 16, 2795–2808. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Pei, Z.; Tian, Y.; He, C. OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation. Mol. Plant Microbe Interact. 2005, 18, 375–384. [Google Scholar] [CrossRef] [PubMed]
- Chern, M.; Fitzgerald, H.A.; Canlas, P.E.; Navarre, D.A.; Ronald, P.C. Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol. Plant Microbe Interact. 2005, 18, 511–520. [Google Scholar] [CrossRef] [PubMed]
- Yuan, Y.; Zhong, S.; Li, Q.; Zhu, Z.; Lou, Y.; Wang, L.; Wang, J.; Wang, M.; Li, Q.; Yang, D.; et al. Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol. J. 2007, 5, 313–324. [Google Scholar] [CrossRef] [PubMed]
- Tang, J.; Zhu, X.; Wang, Y.; Liu, L.; Xu, B.; Li, F.; Fang, J.; Chu, C. Semi-dominant mutations in the CC-NB-LRR-type R gene, NLS1, lead to constitutive activation of defense responses in rice. Plant J. 2011, 66, 996–1007. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.B.; Feng, B.H.; Wang, H.M.; Xu, X.; Shi, Y.F.; He, Y.; Chen, Z.; Sathe, A.P.; Shi, L.; Wu, J.L. A substitution mutation in OsPELOTA confers bacterial blight resistance by activating the salicylic acid pathway. J. Integr. Plant Biol. 2018, 60, 160–172. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Lei, C.L.; Wang, J.L.; Ma, J.; Tang, S.; Wang, C.L.; Zhao, K.J.; Tian, P.; Zhang, H.; Qi, C.Y.; et al. SPL33, encoding an eEF1A-like protein, negatively regulates cell death and defense responses in rice. J. Exp. Bot. 2017, 68, 899–913. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Pan, J.; Cheng, J.; Jiang, G.; Jin, Y.; Gu, Z.; Zhai, W.X.; Ma, B.J. Fine genetic mapping and physical delimitation of the lesion mimic gene spotted leaf 5 (spl5) in rice (Oryza sativa L.). Mol. Breed. 2009, 24, 387–395. [Google Scholar] [CrossRef]
- Chen, X.; Hao, L.; Pan, J.; Zheng, X.; Jiang, G.; Jin, Y.; Gu, Z.M.; Qian, Q.; Zhai, W.X. Spl5, a cell death and defense-related gene, encodes a putative splicing factor 3b subunit 3 (sf3b3) in rice. Mol. Breed. 2012, 30, 939–949. [Google Scholar] [CrossRef]
- Lorrain, S.; Lin, B.; Auriac, M.C.; Kroj, T.; Saindrenan, P.; Nicole, M.; Balagué, C.; Roby, D. VASCULAR ASSOCIATED DEATH1, a novel GRAM domain-containing protein, is a regulator of cell death and defense responses in vascular tissues. Plant Cell. 2004, 16, 2217–2232. [Google Scholar] [CrossRef] [PubMed]
- Noutoshi, Y.; Kuromori, T.; Wada, T.; Hirayama, T.; Kamiya, A.; Imura, Y.; Yasuda, M.; Nakashita, H.; Shirasu, K.; Shinozaki, K. Loss of NECROTIC SPOTTED LESIONS 1 associates with cell death and defense responses in Arabidopsis thaliana. Plant Mol. Biol. 2006, 62, 29–42. [Google Scholar] [CrossRef] [PubMed]
- Mosher, S.; Moeder, W.; Nishimura, N.; Jikumaru, Y.; Joo, S.H.; Urquhart, W.; Klessig, D.F.; Kim, S.K.; Nambara, E.; Yoshioka, K. The lesion-mimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid-dependent manner. Plant Physiol. 2010, 152, 1901–1913. [Google Scholar] [CrossRef] [PubMed]
- Qiao, Y.; Jiang, W.; Lee, J.H.; Park, B.S.; Choi, M.S.; Piao, R.; Woo, M.O.; Roh, J.H.; Han, L.; Paek, N.C.; et al. SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit μ1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa). New Phytol. 2010, 185, 258–274. [Google Scholar] [CrossRef] [PubMed]
- Gray, J.; Close, P.S.; Briggs, S.P.; Johal, G.S. A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 1997, 89, 25–31. [Google Scholar] [CrossRef]
- Yang, M.; Wardzala, E.; Johal, G.S.; Gray, J. The wound-inducible Lls1 gene from maize is an orthologue of the Arabidopsis Acd1 gene, and the LLS1 protein is present in non-photosynthetic tissues. Plant Mol. Biol. 2004, 54, 175–191. [Google Scholar] [CrossRef] [PubMed]
- Mori, M.; Tomita, C.; Sugimoto, K.; Hasegawa, M.; Hayashi, N.; Dubouzet, J.G.; Ochiai, H.; Sekimoto, H.; Hirochika, H.; Kikuchi, S. Isolation and molecular characterization of a Spotted leaf 18 mutant by modified activation-tagging in rice. Plant Mol. Biol. 2007, 63, 847–860. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.H.; Lim, J.H.; Kim, S.S.; Cho, S.H.; Yoo, S.C.; Koh, H.J.; Sakuraba, Y.; Paek, N.C. Mutation of SPOTTED LEAF3 (SPL3) impairs abscisic acid-responsive signaling and delays leaf senescence in rice. J. Exp. Bot. 2015, 66, 7045–7059. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.A.; Cho, K.; Singh, R.; Jung, Y.H.; Jeong, S.H.; Kim, S.H.; Lee, J.E.; Cho, Y.S.; Agrawal, G.K.; Rakwal, R.; et al. Rice OsACDR1 (Oryza sativa accelerated cell death and resistance 1) is a potential positive regulator of fungal disease resistance. Mol. Cells 2009, 28, 431–439. [Google Scholar] [CrossRef] [PubMed]
- Fujiwara, T.; Maisonneuve, S.; Isshiki, M.; Mizutani, M.; Chen, L.; Wong, H.L.; Kawasaki, T.; Shimamoto, K. Sekiguchi lesion gene encodes a cytochrome P450 monooxygenase that catalyzes conversion of tryptamine to serotonin in rice. J. Biol. Chem. 2010, 285, 11308–11313. [Google Scholar] [CrossRef] [PubMed]
- Fekih, R.; Tamiru, M.; Kanzaki, H.; Abe, A.; Yoshida, K.; Kanzaki, E.; Saitoh, H.; Takagi, H.; Natsume, S.; Undan, J.R.; et al. The rice (Oryza sativa L.) LESION MIMIC RESEMBLING, which encodes an AAA-type ATPase, is implicated in defense response. Mol. Genet. Genom. 2015, 290, 611–622. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Ning, Y.; Zhang, Y.; Yu, N.; Zhao, C.; Zhan, X.; Wu, W.; Chen, D.; Wei, X.; Wang, G.L.; et al. OsCUL3a negatively regulates cell death and immunity by degrading OsNPR1 in rice. Plant Cell 2017, 29, 345–359. [Google Scholar] [CrossRef] [PubMed]
- Undan, J.R.; Tamiru, M.; Abe, A.; Yoshida, K.; Kosugi, S.; Takagi, H.; Yoshida, K.; Kanzaki, H.; Saitoh, H.; Fekih, R.; et al. Mutation in OsLMS, a gene encoding a protein with two double-stranded RNA binding motifs, causes lesion mimic phenotype and early senescence in rice (Oryza sativa L.). Genes Genet. Syst. 2012, 87, 169–179. [Google Scholar] [CrossRef] [PubMed]
- Wu, C.; Bordeos, A.; Madamba, M.R.; Baraoidan, M.; Ramos, M.; Wang, G.L.; Leach, J.E.; Leung, H. Rice lesion mimic mutants with enhanced resistance to diseases. Mol. Genet. Genom. 2008, 279, 605–619. [Google Scholar] [CrossRef] [PubMed]
- Jung, Y.H.; Lee, J.H.; Agrawal, G.K.; Rakwal, R.; Kim, J.A.; Shim, J.K.; Lee, S.K.; Jeon, J.S.; Koh, H.J.; Lee, Y.H.; et al. The rice (Oryza sativa) Blast Lesion Mimic Mutant, blm, may confer resistance to blast pathogens by triggering multiple defense-associated signaling pathways. Plant Physiol. Biochem. 2005, 43, 397–406. [Google Scholar] [CrossRef] [PubMed]
- Munnebosch, S.; Alegre, L. Review: Die and let live: Leaf senescence contributes to plant survival under drought stress. Funct. Plant Biol. 2004, 31, 8808–8818. [Google Scholar] [CrossRef]
- Wang, J.; Ye, B.; Yin, J.; Yuan, C.; Zhou, X.; Li, W.; He, M.; Wang, J.; Chen, W.; Qin, P.; et al. Characterization and fine mapping of a light-dependent leaf lesion mimic mutant 1 in rice. Plant Physiol. Biochem. 2015, 97, 44–51. [Google Scholar] [CrossRef] [PubMed]
- Miller, G.; Suzuki, N.; Ciftci-Yilmaz, S.; Mittler, R. Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ. 2010, 33, 453–467. [Google Scholar] [CrossRef] [PubMed]
- Huang, L.; Zhang, H.; Hong, Y.; Liu, S.; Li, D.; Song, F. Stress-responsive expression, subcellular localization and protein-protein interactions of the rice metacaspase family. Int. J. Mol. Sci. 2015, 16, 16216–16241. [Google Scholar] [CrossRef] [PubMed]
- Stegmann, M.; Anderson, R.G.; Ichimura, K.; Pecenkova, T.; Reuter, P.; Žársky, V.; McDowell, J.M.; Shirasu, K.; Trujillo, M. The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. Plant Cell 2012, 24, 4703–4716. [Google Scholar] [CrossRef] [PubMed]
- Wang, D.; Weaver, N.D.; Kesarwani, M.; Dong, X. Induction of protein secretory pathway is required for systemic acquired resistance. Science 2005, 308, 1036–1040. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, A.; Kawasaki, T.; Henmi, K.; ShiI, K.; Kodama, O.; Satoh, H.; Shimamoto, K. Lesion mimic mutants of rice with alterations in early signaling events of defense. Plant J. 1999, 17, 535–545. [Google Scholar] [CrossRef] [PubMed]
- Campbell, M.A.; Ronald, P.C. Characterization of four rice mutants with alterations in the defence response pathway. Mol. Plant Pathol. 2005, 6, 11–21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Noutoshi, Y.; Ito, T.; Seki, M.; Nakashita, H.; Yoshida, S.; Marco, Y.; Shirasu, K.; Shinozaki, K. A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. Plant J. 2005, 43, 873–888. [Google Scholar] [CrossRef] [PubMed]
- Arase, S.; Zhao, C.M.; Akimitsu, K.; Yamamoto, M.; Ichii, M. A recessive lesion mimic mutant of rice with elevated resistance to fungal pathogens. J. Pant Pathol. 2000, 66, 109–116. [Google Scholar] [CrossRef]
- Sindhu, A.; Janick-Buckner, D.; Buckner, B.; Gray, J.; Zehr, U.; Dilkes, B.P.; Johal, G.S. Propagation of cell death in dropdead1, a sorghum ortholog of the maize lls1 mutant. PLoS ONE 2018, 13, e0201359. [Google Scholar] [CrossRef] [PubMed]
- Jacks, T.J.; Davidonis, G.H. Superoxide, hydrogen peroxide, and the respiratory burst of fungally infected plant cells. Mol. Cell. Biochem. 1979, 158, 77–79. [Google Scholar] [CrossRef]
- Shah, J.; Kachroo, P.; Nandi, A.; Klessig, D.F. A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J. 2001, 25, 563–574. [Google Scholar] [CrossRef] [PubMed]
- Prithiviraj, B.; Bais, H.P.; Jha, A.K.; Vivanco, J.M. Staphylococcus aureus pathogenicity on Arabidopsis thaliana is mediated either by a direct effect of salicylic acid on the pathogen or by SA-dependent, NPR1-independent host responses. Plant Ji 2005, 42, 417–432. [Google Scholar] [CrossRef] [PubMed]
- Yang, W.; Xu, X.N.; Li, Y.; Wang, Y.Z.; Li, M.; Wang, Y.; Ding, X.H.; Chu, Z.H. Rutin-mediated priming of plant resistance to three bacterial pathogens initiating the early SA signal pathway. PLoS ONE 2016, 11, e0146910. [Google Scholar] [CrossRef] [PubMed]
- Kunkel, B.N.; Brooks, D.M. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 2002, 5, 325–331. [Google Scholar] [CrossRef]
- He, X.; Jiang, J.S.; Wang, C.Q.; Dehesh, K. ORA59 and EIN3 interaction couples jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF expression. J. Integr. Plant Biol. 2017, 59, 275–287. [Google Scholar] [CrossRef] [PubMed]
- Tao, Z.; Liu, H.; Qiu, D.; Zhou, Y.; Li, X.; Xu, C.; Wang, S. A pair of allelic WRKY genes play opposite role in rice-bacteria interactions. Plant Physiol. 2009, 151, 936–948. [Google Scholar] [CrossRef] [PubMed]
- Shen, X.; Liu, H.; Yuan, B.; Li, X.; Xu, C.; Wang, S. OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. Plant Cell Environ. 2011, 34, 179–191. [Google Scholar] [CrossRef] [PubMed]
- Cutler, S.R.; Rodriguez, P.L.; Finkelstein, R.R.; Abrams, S.R. Abscisic acid: Emergence of a core signaling network. Annu. Rev. Plant Biol. 2010, 61, 651–679. [Google Scholar] [CrossRef] [PubMed]
- Yasuda, M.; Ishikawa, A.; Jikumaru, Y.; Seki, M.; Umezawa, T.; Asami, T.; Maruyama-Nakashita, A.; Kudo, T.; Shinozaki, K.; Yoshida, S.; et al. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 2008, 20, 1678–1692. [Google Scholar] [CrossRef] [PubMed]
- Wu, J.L.; Wu, C.; Lei, C.; Baraoidan, M.; Bordeos, A.; Madamba, M.R.; Ramos-Pamplona, M.; Mauleon, R.; Portugal, A.; Ulat, V.J.; et al. Chemical- and irradiation-induced mutants of indica rice IR64 for forward and reverse genetics. Plant Mol. Biol. 2005, 59, 85–97. [Google Scholar] [CrossRef] [PubMed]
- Wellburn, A.R. The spectral determination of chlorophylls a, and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 1994, 144, 307–313. [Google Scholar] [CrossRef]
- He, Y.; Zhang, Z.H.; Li, L.J.; Tang, S.Q.; Wu, J.-L. Genetic and physio-biochemical characterization of a novel premature senescence leaf mutant in rice (Oryza sativa L.). Int. J. Mol. Sci. 2018, 19, 2339. [Google Scholar] [CrossRef] [PubMed]
- Yin, Z.; Chen, J.; Zeng, L.; Goh, M.; Leung, H.; Khush, G.S.; Wang, G.L. Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol. Plant Microbe Interact. 2000, 13, 869–876. [Google Scholar] [CrossRef] [PubMed]
- Thordal-Christensen, H.; Zhang, Z.G.; Wei, Y.D.; Collinge, D.B. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 1997, 11, 1187–1194. [Google Scholar] [CrossRef]
- Kauffman, H.E. An improved technique for evaluating resistance of rice varieties to Xanthomonas oryzae. Plant Dis. Rep. 1973, 57, 537–541. [Google Scholar]
- Lu, Y.J.; Zheng, K.L. A simple method for DNA extraction in rice. Chin. J. Rice Sci. 1992, 6, 47–48, (In Chinese with an English abstract). [Google Scholar]
Material | Plant Height (cm) | No. Tiller/Plant | Panicle Length (cm) | No. Filled Grain/Panicle | Seed-Setting (%) | 1000-Grain Weight (g) |
---|---|---|---|---|---|---|
IR64 | 117.0 ± 0.5 | 19.3 ± 3.2 | 26.4 ± 0.2 | 58.0 ± 3.6 | 50.4 ± 1.1 | 24.3 ± 0.2 |
spl24 | 109.8 ± 1.3 ** | 28.0 ± 1.0 * | 25.6 ± 0.6 * | 69.3 ± 2.5 * | 55.6 ± 0.6 ** | 22.9 ± 0.3 ** |
Lesion length (cm) | |||
---|---|---|---|
race | IR24 | IR64 | spl24 |
HB17 | 25.39 ± 3.85 | 5.71 ± 1.06 | 3.70 ± 1.39 * |
GD1358 | 12.87 ± 0.51 | 5.60 ± 1.28 | 4.40 ± 1.68 |
PXO71 | 23.10 ± 4.71 | 3.05 ± 0.33 | 2.43 ± 0.93 |
JS97-2 | 16.48 ± 2.29 | 12.40 ± 1.41 | 7.00 ± 1.96 ** |
PXO112 | 23.93 ± 2.86 | 4.82 ± 0.88 | 3.40 ± 0.89 ** |
Zhe173 | 19.98 ± 3.07 | 7.01 ± 1.02 | 4.80 ± 1.43 ** |
OS-225 | 14.32 ± 2.92 | 2.41 ± 0.67 | 2.40 ± 0.57 |
PXO339 | 22.14 ± 2.32 | 16.63 ± 2.01 | 9.20 ± 1.95 ** |
PXO347 | 21.40 ± 3.67 | 18.15 ± 2.11 | 10.10 ± 1.66 ** |
PXO349 | 17.68 ± 2.71 | 13.17 ± 1.80 | 9.40 ± 2.20 ** |
ORF | Gene ID | Annotation |
---|---|---|
ORF1 | LOC_Os11g34460 | OsFBO10-F-box and other domain containing protein, expressed |
ORF2 | LOC_Os11g34470 | expressed protein |
ORF3 | LOC_Os11g34570 | lysM domain containing GPI-anchored protein precursor, putative, expressed |
ORF4 | LOC_Os11g34580 | hypothetical protein |
ORF5 | LOC_Os11g34610 | DUF26 kinases have homology to DUF26 containing loci, expressed |
ORF6 | LOC_Os11g34624 | DUF26 kinases have homology to DUF26 containing loci, expressed |
ORF7 | LOC_Os11g34640 | expressed protein |
ORF8 | LOC_Os11g34650 | expressed protein |
ORF9 | LOC_Os11g34660 | Protease inhibitor/seed storage/LTP family protein precursor, expressed |
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Chen, Z.; Chen, T.; Sathe, A.P.; He, Y.; Zhang, X.-b.; Wu, J.-l. Identification of a Novel Semi-Dominant Spotted-Leaf Mutant with Enhanced Resistance to Xanthomonas oryzae pv. oryzae in Rice. Int. J. Mol. Sci. 2018, 19, 3766. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms19123766
Chen Z, Chen T, Sathe AP, He Y, Zhang X-b, Wu J-l. Identification of a Novel Semi-Dominant Spotted-Leaf Mutant with Enhanced Resistance to Xanthomonas oryzae pv. oryzae in Rice. International Journal of Molecular Sciences. 2018; 19(12):3766. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms19123766
Chicago/Turabian StyleChen, Zheng, Ting Chen, Atul Prakash Sathe, Yuqing He, Xiao-bo Zhang, and Jian-li Wu. 2018. "Identification of a Novel Semi-Dominant Spotted-Leaf Mutant with Enhanced Resistance to Xanthomonas oryzae pv. oryzae in Rice" International Journal of Molecular Sciences 19, no. 12: 3766. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms19123766