白叶枯病菌和细菌性条斑病菌多样性的TALE效应 蛋白调控水稻抗（感）病性机理与利用策略

doi:10.3864/j.issn.0578-1752.2013.14.005

Abstract

Abstract: Breeding and planting resistant rice varieties is one of the most effective and economic ways to control bacterial leaf blight and bacterial leaf streak diseases caused by Xanthomonas oryzae pv. oryzae (Xoo) and pv. oryzicola (Xoc), respectively. Recent land-marked advances in understanding the mechanism of rice resistance (R) or susceptibility(S) manipulated by transcriptional activator-like effector (TALEs) of Xoo and Xoc shall definitely alter present strategies in rice breeding for disease resistance. Hereby, the authors reviewed the corresponding relationships between known TALEs of a Xoo model strain PXO99A and known and unknown R or S genes in rice, forwarded the prospects regarding to co-evolution of new tale genes in the pathogens and to mine R or S genes in rice, and introduced a TALEN technology, developed based on DNA-binding specificity of TALEs, that has been used to genetically transfer a susceptible rice line into a resistant one. The TALEN technology is tremendously a powerful tool that will realize such a goal in altering susceptible rice varieties (materials) with high yield and high quality into resistant ones with high yield and high quality.

Key words: rice , Xanthomonas oryzae , TALE effector , resistance (susceptibility) mechanism , TALEN

LI Zheng, XIONG Li, JI Zhi-Yuan, ZOU Li-Fang, ZOU Hua-Song, CHEN Gong-You. Mechanisms of Rice Resistance (Susceptibility) Manipulated by Diverse TALEs of Xanthomonas oryzae pv. oryzae and pv. oryzicola and Potential Utilization in Rice Breeding[J].Scientia Agricultura Sinica, 2013, 46(14): 2894-2901.

0
/ / Recommend

Add to citation manager EndNote|Reference Manager|ProCite|BibTeX|RefWorks

URL: https://www.chinaagrisci.com/EN/10.3864/j.issn.0578-1752.2013.14.005

https://www.chinaagrisci.com/EN/Y2013/V46/I14/2894

References

[1]Zou H S, Yuan L, Guo W, Li Y R, Che Y Z, Zou L F, Chen G Y. Construction of a Tn5-tagged mutant library of Xanthomonas oryzae pv. oryzicola as an invaluable resource for functional genomics. Current Microbiology, 2011, 62(3): 908-916.

[2]Li Y R, Zou H S, Che Y Z, Cui Y P, Guo W, Zou L F, Chatterjee S, Biddle E M, Yang C H, Chen G Y. A novel regulatory role of HrpD6 in regulating hrp-hrc-hpa genes in Xanthomonas oryzae pv. oryzicola. Molecular Plant-Microbe Interactions, 2011, 24(9): 1086-1101.

[3]Li Y R, Che Y Z, Zou H S, Cui Y P, Guo W, Zou L F, Biddle E M, Yang C H, Chen G Y. Hpa2 required by HrpF to translocate Xanthomonas oryzae transcriptional activator-like effectors into rice for pathogenicity. Applied and Environmental Microbiology, 2011, 77(11): 3809-3818.

[4]Ronald P, Leung H. The most precious things are not jade and pearls. Science, 2002, 296(5565): 58-59.

[5]Shimamoto K, Kyozuka J. Rice as a model for comparative genomics of plants. Annual Review of Plant Biology, 2002, 53(1): 399-419.

[6]Ochiai H, Inoue Y, Takeya M, Sasaki A, Kaku H. Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Japan Agricultural Research Quarterly, 2005, 39(4): 275-287.

[7]Lee B M, Park Y J, Park D S, Kang H W, Kim J G, Song E S, Park I C, Yoon U H, Hahn J H, Koo B S, Lee G B, Kim H, Park H S, Yoon K O, Kim J H, Jung C H, Koh N H, Seo J S, Go S J. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Research, 2005, 33(2): 577-586.

[8]Salzberg S L, Sommer D D, Schatz M C, Phillippy A M, Rabinowicz P D, Tsuge S, Furutani A, Ochiai H, Delcher A L, Kelley D, Madupu R, Puiu D, Radune D, Shumway M, Trapnell C, Aparna G, Jha G, Pandey A, Patil P B, Ishihara H, Meyer D F, Szurek B, Verdier V, Koebnik R, Dow J M, Ryan R P, Hirata H, Tsuyumu S, Won Lee S, Seo Y S, Sriariyanum M, Ronald P C, Sonti R V, Van Sluys M A, Leach J E, White F F, Bogdanove A J. Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics, 2008, 9(1): 204.

[9]Bogdanove A J, Koebnik R, Lu H, Furutani A, Angiuoli S V, Patil P B, Van Sluys M A, Ryan R P, Meyer D F, Han S W, Aparna G, Rajaram M, Delcher A L, Phillippy A M, Puiu D, Schatz M C, Shumway M, Sommer D D, Trapnell C, Benahmed F, Dimitrov G, Madupu R, Radune D, Sullivan S, Jha G, Ishihara H, Lee S W, Pandey A, Sharma V, Sriariyanun M, Szurek B, Vera-Cruz C M, Dorman K S, Ronald P C, Verdier V, Dow J M, Sonti R V, Tsuge S, Brendel V P, Rabinowicz P D, Leach J E, White F F, Salzberg S L. Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp.. Journal of Bacteriology, 2011, 193(19): 5450-5464.

[10]Nino-Liu D O, Ronald P C, Bogdanove A J. Xanthomonas oryzae pathovars: model pathogens of a model crop. Molecular Plant Pathology, 2006, 7(5): 303-324.

[11]Zou L, Wang X, Xiang Y, Zhang B, Li Y R, Xiao Y, Wang J, Walmsley A R, Chen G. Elucidation of the hrp clusters of Xanthomonas oryzae pv. oryzicola that control the hypersensitive response in nonhost tobacco and pathogenicity in susceptible host rice. Applied and Environmental Microbiology, 2006, 72(9): 6212-6224.

[12]Zipfel C. Early molecular events in PAMP-triggered immunity. Current Opinion in Plant Biology, 2009, 12(4): 414-420.

[13]Zipfel C. Pattern-recognition receptors in plant innate immunity. Current Opinion in Immunology, 2008, 20(1): 10-16.

[14]Boller T, He S Y. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 2009, 324(5928): 742-744.

[15]Gao M, Wang X, Wang D, Xu F, Ding X, Zhang Z, Bi D, Cheng Y T, Chen S, Li X, Zhang Y. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host & Microbe, 2009, 6(1): 34-44.

[16]Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nature Immunology, 2010, 11(5): 373-384.

[17]Zhao B, Ardales E Y, Raymundo A, Bai J, Trick H N, Leach J E, Hulbert S H. The avrRxo1 gene from the rice pathogen Xanthomonas oryzae pv. oryzicola confers a nonhost defense reaction on maize with resistance gene Rxo1. Molecular Plant-Microbe Interactions, 2004, 17(7): 771-779.

[18]Lee S W, Han S W, Sririyanum M, Park C J, Seo Y S, Ronald P C. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science Signaling, 2009, 326(5954): 850-853.

[19]Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert S. A maize resistance gene functions against bacterial streak disease in rice. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(43): 15383-15388.

[20]Zhou Y L, Xu M R, Zhao M F, Xie X W, Zhu L H, Fu B Y, Li Z K. Genome-wide gene responses in a transgenic rice line carrying the maize resistance gene Rxo1 to the rice bacterial streak pathogen, Xanthomonas oryzae pv. oryzicola. BMC Genomics, 2010, 11(1): 78.

[21]Song W Y, Wang G L, Chen L L, Kim H S, Pi L Y, Holsten T, Gardner J, Wang B, Zhai W X, Zhu L H, Fauquet C, Ronald P. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science-AAAS-Weekly Paper Edition, 1995, 270(5243): 1804-1806.

[22]Song W Y, Pi L Y, Wang G L, Gardner J, Holsten T, Ronald P C. Evolution of the rice Xa21 disease resistance gene family. The Plant Cell, 1997, 9(8): 1279-1287.

[23]Boch J, Bonas U. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annual Review of Phytopathology, 2010, 48: 419-436.

[24]Bogdanove A J, Schornack S, Lahaye T. TAL effectors: finding plant genes for disease and defense. Current Opinion in Plant Biology, 2010, 13(4): 394-401.

[25]Scholze H, Boch J. TAL effectors are remote controls for gene activation. Current Opinion in Microbiology, 2011, 14(1): 47-53.

[26]Jiang W, Jiang B L, Xu R Q, Huang J D, Wei H Y, Jiang G F, Cen W J, Liu J, Ge Y Y, Li G H, Su L L, Hang X H, Tang D J, Lu G T, Feng J X, He Y Q, Tang J L. Identification of six type III effector genes with the PIP box in Xanthomonas campestris pv. campestris and five of them contribute individually to full pathogenicity. Molecular Plant-Microbe Interactions, 2009, 22(11): 1401-1411.

[27]Song C, Yang B. Mutagenesis of 18 type III effectors reveals virulence function of XopZPXO99 in Xanthomonas oryzae pv. oryzae. Molecular Plant-Microbe Interactions, 2010, 23(7): 893-902.

[28]Bonas U, Van den Ackerveken G. Gene-for-gene interactions: bacterial avirulence proteins specify plant disease resistance. Current Opinion in Microbiology, 1999, 2(1): 94-98.

[29]Bai J, Choi S H, Ponciano G, Leung H, Leach J E. Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. Molecular Plant-Microbe Interactions, 2000, 13(12): 1322-1329.

[30]Wu X, Li Y, Zou L, Chen G. Gene-for-gene relationships between rice and diverse avrBs3/pthA avirulence genes in Xanthomonas oryzae pv. oryzae. Plant Pathology, 2007, 56(1): 26-34.

[31]Fujikawa T, Ishihara H, Leach J E, Tsuyumu S. Suppression of defense response in plants by the avrBs3/pthA gene family of Xanthomonas spp.. Molecular Plant-Microbe Interactions, 2006, 19(3): 342-349.

[32]Chen L Q, Hou B H, Lalonde S, Takanaga H, Hartung M L, Qu X Q, Guo W J, Kim J G, Underwood W, Chaudhuri B. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature, 2010, 468(7323): 527-532.

[33]Yu Y, Streubel J, Balzergue S, Champion A, Boch J, Koebnik R, Feng J, Verdier V, Szurek B. Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. Molecular Plant-Microbe Interactions, 2011, 24(9): 1102-1113.

[34]Yang B, Sugio A, White F F. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(27): 10503-10508.

[35]Yuan M, Chu Z, Li X, Xu C, Wang S. Pathogen-induced expressional loss of function is the key factor in race-specific bacterial resistance conferred by a recessive R gene xa13 in rice. Plant and Cell Physiology, 2009, 50(5): 947-955.

[36]Römer P, Recht S, Strauß T, Elsaesser J, Schornack S, Boch J, Wang S, Lahaye T. Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen, Xanthomonas oryzae pv. oryzae. New Phytologist, 2010, 187(4): 1048-1057.

[37]Antony G, Zhou J, Huang S, Li T, Liu B, White F, Yang B. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. The Plant Cell, 2010, 22(11): 3864-3876.

[38]Zou H S, Zhao W X, Zhang X F, Han Y C, Zou L F, Chen G Y. Identification of an avirulence gene, avrxa5, from the rice pathogen Xanthomonas oryzae pv. oryzae. Science China Life Sciences, 2010, 53(12): 1440-1449.

[39]Yang B, Zhu W, Johnson L B, White F F. The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway- dependent nuclear-localized double-stranded DNA-binding protein. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97(17): 9807-9812.

[40]Zhu W, Yang B, Wills N, Johnson L B, White F F. The C terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP16 from the herpes simplex virus. The Plant Cell, 1999, 11(9): 1665-1674.

[41]Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang G L, White F F. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature, 2005, 435(7045): 1122-1125.

[42]Wang C L, Xu A B, Gao Y, Fan Y L, Liang Y T, Zheng C K, Sun L Q, Wang W Q, Zhao K J. Generation and characterisation of Tn5-tagged Xanthomonas oryzae pv. oryzae mutants that overcome Xa23- mediated resistance to bacterial blight of rice. European Journal of Plant Pathology, 2009, 123(3): 343-351.

[43]Sugio A, Yang B, Zhu T, White F F. Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAγ1 and OsTFX1 during bacterial blight of rice. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(25): 10720-10725.

[44]邹丽芳, 陈功友, 武晓敏, 王金生. 中国水稻条斑病细菌 avrBs3/PthA 家族基因的克隆和序列分析. 中国农业科学, 2005, 38(5): 929-935.

Zou L F, Chen G Y, Wu X M, Wang J S. Cloning and sequence analysis of diverse members of avrBs3/PthA family of Xanthomonas oryzae pv. oryzicola. China Agriculture Science, 2005, 38(5): 929-935. (in Chinese)

[45]陈功友, 邹丽芳, 武晓敏, 李玉蓉, 王金生. 水稻条斑病细菌中新发现的 avrBs3/PthA家族新成员avr/pth13基因. 中国水稻科学, 2005, 19(4): 291-296.

Chen G Y, Zou L F, Wu X M, Li Y R, Wang J S. avr/pth13 gene of Xanthomonas oryzae pv. oryzicola, a novel virulence member of avrBs3/PthA family, strengthening virulence of Xanthomonas oryzae pv. oryzae on rice. Chinese Journal of Rice Science, 2005, 19(4): 291-296. (in Chinese)

[46]Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U. Breaking the code of DNA binding specificity of TAL-Type III effectors. Science, 2009, 326(5959): 1509-1512.

[47]Moscou M J, Bogdanove A J. A simple cipher governs DNA recognition by TAL effectors. Science, 2009, 326(5959): 1501.

[48]Deng D, Yan C, Pan X, Mahfouz M, Wang J, Zhu J K, Shi Y, Yan N. Structural basis for sequence-specific recognition of DNA by TAL effectors. Science, 2012, 335(6069): 720-723.

[49]Mak A N, Bradley P, Cernadas R A, Bogdanove A J, Stoddard B L. The crystal structure of TAL effector PthXo1 bound to its DNA target. Science, 2012, 335(6069): 716-719.

[50]纪志远, 杨娟, 王寅鹏, 周丹, 李玉蓉, 邹丽芳, 陈功友. 中国水稻白叶枯病菌小种 C8 菌株无毒基因的分离及功能鉴别. 中国水稻科学, 2009, 23(5): 463-469.

Ji Z Y, Yang J, Wang Y P, Zhou D, Li Y R, Zou Y F, Chen G Y. Identification of a specific avirulence gene from Chinese race C8 of Xanthomonas oryzae pv. oryzae. Chinese Journal of Rice Science, 2009, 23(5): 463-469. (in Chinese)

[51]曹燕飞, 邹丽芳, 赵文祥, 纪志远, 邹华松, 陈功友. 水稻条斑病菌 avrBs3/pthA 家族基因敲除体系的建立. 浙江大学学报: 农业与生命科学版, 2011, 37(1): 40-48.

Cao Y F, Zou L F, Zhao W X, Ji Z Y, Zou H S, Chen G Y. Establishment of knockout mutagenesis in avrBs3/pthA family genes of Xanthomonas oryzae pv. oryzicola. Journal of Zhejiang University: Agriculture & Life Sciences, 2011, 37(1): 40-48. (in Chinese)

[52]Li T, Huang S, Zhao X F, Wright D A, Carpenter S, Spalding M H, Weeks D P, Yang B. Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Research, 2011, 39(14): 6315-6325.

[53]Miller J C, Tan S, Qiao G, Barlow K A, Wang J, Xia D F, Meng X, Paschon D E, Leung E, Hinkley S J. A TALE nuclease architecture for efficient genome editing. Nature Biotechnology, 2011, 29(2): 143-148.

[54]Morbitzer R, Roemer P, Boch J, Lahaye T. Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(50): 21617-21622.

[55]Cermak T, Doyle E L, Christian M, Wang L, Zhang Y, Schmidt C, Baller J A, Somia N V, Bogdanove A J, Voytas D F. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Research, 2011, 39(12): e82.

[56]Mahfouz M M, Li L X, Shamimuzzaman M, Wibowo A, Fang X Y, Zhu J K. De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(6): 2623-2628.

[57]Morbitzer R, Elsaesser J, Hausner J, Lahaye T. Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Research, 2011, 39(13): 5790-5799.

[58]Li T, Liu B, Spalding M H, Weeks D P, Yang B. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nauret Biotechnology, 2012, 30(5): 390-392.

Metrics

Viewed

Full text

Abstract

Cited

Shared

Discussed

Comments

Recommended 0

No Suggested Reading articles found!

Mechanisms of Rice Resistance (Susceptibility) Manipulated by Diverse TALEs of Xanthomonas oryzae pv. oryzae and pv. oryzicola and Potential Utilization in Rice Breeding

PDF

Cited

Abstract

Cite this article

share this article

References

Related Articles 15

Metrics

Comments

Recommended 0

[1]	XIAO DeShun, XU ChunMei, WANG DanYing, ZHANG XiuFu, CHEN Song, CHU Guang, LIU YuanHui. Effects of Rhizosphere Oxygen Environment on Phosphorus Uptake of Rice Seedlings and Its Physiological Mechanisms in Hydroponic Condition [J]. Scientia Agricultura Sinica, 2023, 56(2): 236-248.
[2]	ZHANG XiaoLi, TAO Wei, GAO GuoQing, CHEN Lei, GUO Hui, ZHANG Hua, TANG MaoYan, LIANG TianFeng. Effects of Direct Seeding Cultivation Method on Growth Stage, Lodging Resistance and Yield Benefit of Double-Cropping Early Rice [J]. Scientia Agricultura Sinica, 2023, 56(2): 249-263.
[3]	ZHANG Wei,YAN LingLing,FU ZhiQiang,XU Ying,GUO HuiJuan,ZHOU MengYao,LONG Pan. Effects of Sowing Date on Yield of Double Cropping Rice and Utilization Efficiency of Light and Heat Energy in Hunan Province [J]. Scientia Agricultura Sinica, 2023, 56(1): 31-45.
[4]	FENG XiangQian,YIN Min,WANG MengJia,MA HengYu,CHU Guang,LIU YuanHui,XU ChunMei,ZHANG XiuFu,ZHANG YunBo,WANG DanYing,CHEN Song. Effects of Meteorological Factors on Quality of Late Japonica Rice During Late Season Grain Filling Stage Under ‘Early Indica and Late Japonica’ Cultivation Pattern in Southern China [J]. Scientia Agricultura Sinica, 2023, 56(1): 46-63.
[5]	SANG ShiFei,CAO MengYu,WANG YaNan,WANG JunYi,SUN XiaoHan,ZHANG WenLing,JI ShengDong. Research Progress of Nitrogen Efficiency Related Genes in Rice [J]. Scientia Agricultura Sinica, 2022, 55(8): 1479-1491.
[6]	GUI RunFei,WANG ZaiMan,PAN ShengGang,ZHANG MingHua,TANG XiangRu,MO ZhaoWen. Effects of Nitrogen-Reducing Side Deep Application of Liquid Fertilizer at Tillering Stage on Yield and Nitrogen Utilization of Fragrant Rice [J]. Scientia Agricultura Sinica, 2022, 55(8): 1529-1545.
[7]	LIAO Ping,MENG Yi,WENG WenAn,HUANG Shan,ZENG YongJun,ZHANG HongCheng. Effects of Hybrid Rice on Grain Yield and Nitrogen Use Efficiency: A Meta-Analysis [J]. Scientia Agricultura Sinica, 2022, 55(8): 1546-1556.
[8]	HAN XiaoTong,YANG BaoJun,LI SuXuan,LIAO FuBing,LIU ShuHua,TANG Jian,YAO Qing. Intelligent Forecasting Method of Rice Sheath Blight Based on Images [J]. Scientia Agricultura Sinica, 2022, 55(8): 1557-1567.
[9]	GAO JiaRui,FANG ShengZhi,ZHANG YuLing,AN Jing,YU Na,ZOU HongTao. Characteristics of Organic Nitrogen Mineralization in Paddy Soil with Different Reclamation Years in Black Soil of Northeast China [J]. Scientia Agricultura Sinica, 2022, 55(8): 1579-1588.
[10]	ZHU DaWei,ZHANG LinPing,CHEN MingXue,FANG ChangYun,YU YongHong,ZHENG XiaoLong,SHAO YaFang. Characteristics of High-Quality Rice Varieties and Taste Sensory Evaluation Values in China [J]. Scientia Agricultura Sinica, 2022, 55(7): 1271-1283.
[11]	ZHAO Ling, ZHANG Yong, WEI XiaoDong, LIANG WenHua, ZHAO ChunFang, ZHOU LiHui, YAO Shu, WANG CaiLin, ZHANG YaDong. Mapping of QTLs for Chlorophyll Content in Flag Leaves of Rice on High-Density Bin Map [J]. Scientia Agricultura Sinica, 2022, 55(5): 825-836.
[12]	JIANG JingJing,ZHOU TianYang,WEI ChenHua,WU JiaNing,ZHANG Hao,LIU LiJun,WANG ZhiQin,GU JunFei,YANG JianChang. Effects of Crop Management Practices on Grain Quality of Superior and Inferior Spikelets of Super Rice [J]. Scientia Agricultura Sinica, 2022, 55(5): 874-889.
[13]	ZHANG YaLing, GAO Qing, ZHAO Yuhan, LIU Rui, FU Zhongju, LI Xue, SUN Yujia, JIN XueHui. Evaluation of Rice Blast Resistance and Genetic Structure Analysis of Rice Germplasm in Heilongjiang Province [J]. Scientia Agricultura Sinica, 2022, 55(4): 625-640.
[14]	WANG YaLiang,ZHU DeFeng,CHEN RuoXia,FANG WenYing,WANG JingQing,XIANG Jing,CHEN HuiZhe,ZHANG YuPing,CHEN JiangHua. Beneficial Effects of Precision Drill Sowing with Low Seeding Rates in Machine Transplanting for Hybrid Rice to Improve Population Uniformity and Yield [J]. Scientia Agricultura Sinica, 2022, 55(4): 666-679.
[15]	CHEN TingTing, FU WeiMeng, YU Jing, FENG BaoHua, LI GuangYan, FU GuanFu, TAO LongXing. The Photosynthesis Characteristics of Colored Rice Leaves and Its Relation with Antioxidant Capacity and Anthocyanin Content [J]. Scientia Agricultura Sinica, 2022, 55(3): 467-478.