Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (16): 3393-3405.doi: 10.3864/j.issn.0578-1752.2021.16.003

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Genetic Diversity Analysis of Rhizobia Associated with Medicago sativa Cultivated in Northeast and North China

LI XinYuan(),LOU JinXiu,LIU QingYuan,HU Jian(),ZHANG YingJun   

  1. College of Agro-grassland Science, Nanjing Agricultural University, Nanjing 210095
  • Received:2021-02-03 Accepted:2021-05-02 Online:2021-08-16 Published:2021-08-24
  • Contact: Jian HU E-mail:nalxy0806@163.com;jaffyhu@njau.edu.cn

Abstract:

【Objective】Medicago sativa is reputed to be the “Queen of Forages”, its cultivated area has increased in Northeast and North China in recent years. However, the quality and yield of M. sativa still do not meet the needs of livestock husbandry development in China. The objective of this study was to analyze the genetic diversity of rhizobia associated with M. sativa from Northeast and North China, which will provide valuable reference for screening and applying high efficient nitrogen fixing rhizobia from M. sativa.【Method】Surface sterilization and plate streaking method were used to recover and purify the rhizobia from M. sativa root nodules; BOX-PCR was applied to identify the genotypes of the tested rhizobia; Three housekeeping (atpD, glnII and rpoB) and two symbiotic genes (nodC and nifH) were selected for phylogenetic analysis of the representative genotypes. 【Result】A total of 499 rhizobia strains were obtained from 19 sampling regions located in Northeast and North China. All strains were classified into 37 BOX types. The BOX types showed a strong geographic distribution, and host cultivars imposed a certain selection pressure to the genotypes of rhizobia. 97.60% (487/499) of the strains was identified as Sinorhizobium meliloti, while the rest 12 strains were identified as S. adhaerens, Mesorhizobium huakuii, Rhizobium loessense, R. mesosinicum, R. vignae, Mesorhizobium sp. and Phyllobacterium sp.. All the 12 strains were collected from Northeast China, while all strains from North China were S. meliloti. The housekeeping genes revealed similar phylogenetic trends when they were used for inter-species analysis, but revealed differently for intra-species analysis. Phylogeny of symbiotic genes revealed that horizontal gene transfer happened between genera and species within genus. nifH showed high genetic diversity than nodC in S. meliloti strains.【Conclusion】 Rhizobia associated with M. sativa from Northeast and North China showed high genetic diversity, moreover, they had a strong characteristics of geographic distribution and host selection.

Key words: Medicago sativa, Sinorhizobium meliloti, genetic diversity, phylogeny, horizontal transfer

Table 1

The information of rhizobia associated with Medicago sativa in this study"

采样地
Sampling site
省份
Province
区域
Region
采样时间
Sampling date (Y.M)
寄主品种
Host cultivar
菌株数量
No. of strains
五河Wuhe 安徽Anhui 华北North 2016.1 未知Unknown 58
沧州Cangzhou 河北Hebei 华北North 2017.5 中苜1号、中苜3号、甘农3号
Zhongmu1, Zhongmu3, Gannong3
32
衡水Hengshui 河北Hebei 华北North 2017.5 中苜1号、WL363 Zhongmu1, WL363 48
新乡Xinxiang 河南Henan 华北North 2017.5 M343、M354 58
荥阳Xingyang 河南Henan 华北North 2017.5 三得利 Sandeli 20
郑州Zhengzhou 河南Henan 华北North 2017.5 劲能5010 Jinneng5010 32
齐齐哈尔Qiqihar 黑龙江Heilongjiang 东北Northeast 2015.9 806 11
白城Baicheng 吉林Jilin 东北Northeast 2017.5 公农5号 Gongnong5 59
前郭Qianguo 吉林Jilin 东北Northeast 2015.9 敖汉 Aohan 9
通榆Tongyu 吉林Jilin 东北Northeast 2015.9 东苜1号 Dongmu1 16
延边Yanbian 吉林Jilin 东北Northeast 2015.9 公农1号 Gongnong1 4
凤城Fengcheng 辽宁Liaoling 东北Northeast 2016.6 未知 Unknown 6
建平Jianping 辽宁Liaoning 东北Northeast 2016.6 未知 Unknown 12
辽阳Liaoyang 辽宁Liaoning 东北Northeast 2016.6 龙牧、WL319 Longmu, WL319 34
沈阳Shenyang 辽宁Liaoning 东北Northeast 2016.6 公农1号 Gonglong1 32
特尼河Turney river 内蒙古Inner Mongolia 东北Northeast 2016.1 未知 Unknown 7
谢尔塔拉Cher tara 内蒙古Inner Mongolia 东北Northeast 2015.9 未知 Unknown 9
胶州Jiaozhou 山东Shandong 华北North 2017.6 三得利、中苜3号 Sandeli, Zhongmu3 24
聊城Liaocheng 山东Shandong 华北North 2017.6 三得利、WL363 Sandeli, WL363 28
总计 Total 499

Table 2

The BOX types and their distributions in the rhizobia associated with Medicago sativa"

BOX型
BOX type
菌株数
No. of strains
占比
Percentage (%)
比对序列号
Accession No.
菌种
Species
采样地b
Sampling site
区域
Region
1 38 7.62 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城、凤城、黑龙江(5)b、建平(6)、辽阳(21)、前郭、沈阳、五河(2)
Baicheng, Fengcheng, Heilongjiang (5), Jianping (6), Liaoyang (21), Qianguo, Shenyang, Wuhe (2)
NE、N
2 2 0.40 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城、五河
Baicheng, Wuhe
NE、N
3 1 0.20 EF549450
(91.34) a
中慢生根瘤菌属
Mesorhizobium sp.
白城
Baicheng
NE
4 1 0.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
辽阳
Liaoyang
NE
5 6 1.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城、前郭、特尼河、通榆(2)、五河
Baicheng, Qianguo, Turney river, Tongyu (2), Wuhe
NE、N
6 1 0.20 KF206625
(100)
黄土根瘤菌
Rhizobium loessense
白城
Baicheng
NE
7 93 18.64 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城(2)、沧州、衡水(28)、新乡(23)、荥阳、郑州(13)、辽阳(10)、前郭(2)、聊城(3)、沈阳(7)、五河(3)
Baicheng (2), Cangzhou, Hengshui (28), Xinxiang (23), Xingyang, Zhengzhou (13), Liaoyang (10), Qianguo (2), Liaocheng (3), Shenyang (7), Wuhe (3)
NE、N
8 2 0.40 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城、沈阳
Baicheng, Shenyang
NE
9 3 0.60 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城、郑州、齐齐哈尔
Baicheng, Zhengzhou, Qiqihar
NE、N
10 1 0.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城
Baicheng
NE
11 1 0.20 KF206625
(100)
黄土根瘤菌
Rhizobium loessense
白城
Baicheng
NE
12 4 0.80 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城、聊城(3)
Baicheng, Liaocheng (3)
NE、N
13 15 3.00 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城(5)、建平、通榆(4)、谢尔塔拉(4)、延边
Baicheng (5), Jianping, Tongyu (4), Cher tara (4), Yanbian
NE
14 8 1.60 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城、前郭、通榆(3)、五河(2)、延边
Baicheng, Qianguo, Tongyu (3), Wuhe (2), Yanbian
NE、N
15 1 0.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城
Baicheng
NE
16 2 0.40 KP251033
(100)
华癸根瘤菌
Mesorhizobium huakuii
通榆
Tongyu
NE
17 1 0.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
前郭
Qianguo
NE
18 15 3.00 - 草木樨中华根瘤菌
Sinorhizobium meliloti
齐齐哈尔(3)、沈阳、特尼河(3)、五河(6)、谢尔塔拉(2)
Qiqihar (3), Shenyang, Turney river (3), Wuhe (6), Cher tara (2)
NE、N
19 36 7.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
沧州、衡水(5)、新乡(2)、荥阳(2)、郑州(5)、前郭、胶州(12)、通榆(2)、五河(4)、延边(2)
Cangzhou, Hengshui (5), Xinxiang (2), Xingyang (2), Zhengzhou (5), Qianguo, Jiaozhou (12), Tongyu (2), Wuhe (4), Yanbian (2)
NE、N
20 13 2.60 - 草木樨中华根瘤菌
Sinorhizobium meliloti
齐齐哈尔、沈阳(8)、通榆 、五河(3)
Qiqihar, Shenyang (8), Tongyu, Wuhe (3)
NE、N
21 1 0.20 AM418747
(99.67)
附着剑菌
Sinorhizobium adhaerens
沈阳
Shenyang
NE
OX型
BOX type
菌株数
No. of strains
占比
Percentage (%)
比对序列号
Accession No.
菌种
Species
采样地b
Sampling site
区域
Region
22 58 11.62 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城(35)、凤城(2)、齐齐哈尔、建平(4)、前郭、沈阳(8)、五河(5)、谢尔塔拉(2)
Baicheng (35), Fengcheng (2), Qiqihar, Jianping (4), Qianguo, Shenyang (8), Wuhe (5), Cher tara (2)
NE、N
23 141 28.26 - 草木樨中华根瘤菌
Sinorhizobium meliloti
凤城(3)、沧州(25)、衡水(14)、新乡(20)、荥阳(14)、郑州(12)、辽阳(2)、胶州(12)、聊城(20)、沈阳、通榆(2)、五河(15)、谢尔塔拉
Fengcheng (3), Cangzhou (25), Hengshui (14), Xinxiang (20), Xingyang (14), Zhengzhou (12), Liaoyang (2), Jiaozhou (12), Liaocheng (20), Shenyang, Tongyu (2), Wuhe (15), Cher tara
NE、N
24 8 1.60 - 草木樨中华根瘤菌
Sinorhizobium meliloti
五河
Wuhe
N
25 3 0.60 - 草木樨中华根瘤菌
Sinorhizobium meliloti
荥阳(2)、前郭
Xingyang (2), Qianguo
NE、N
26 1 0.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
五河
Wuhe
N
27 4 0.80 - 草木樨中华根瘤菌
Sinorhizobium meliloti
特尼河(3)、五河
Turney river (3), Wuhe
NE、N
28 6 1.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
荥阳、建平、五河(4)
Xingyang, Jianping, Wuhe (4)
NE、N
29 3 0.60 - 草木樨中华根瘤菌
Sinorhizobium meliloti
白城(2)、谢尔塔拉
Baicheng (2), Cher tara
NE
30 1 0.20 EU120727
(98.01)
华中根瘤菌
Rhizobium mesosinicum
沈阳
Shenyang
NE
31 2 0.40 AM418747
(99.67)
附着剑菌
Sinorhizobium adhaerens
沈阳
Shenyang
NE
32 1 0.20 KF580979
(92.72)
芸苔叶杆菌
Phyllobacterium brassicacearum
沈阳
Shenyang
NE
33 19 3.81 - 草木樨中华根瘤菌
Sinorhizobium meliloti
沧州(4)、新乡(11)、郑州、聊城(2)
Cangzhou (4), Xinxiang (11), Zhengzhou, Liaocheng (2)
N
34 2 0.40 - 草木樨中华根瘤菌
Sinorhizobium meliloti
新乡
Xinxiang
N
35 1 0.20 - 草木樨中华根瘤菌
Sinorhizobium meliloti
沧州
Cangzhou
N
36 1 0.20 KF206603
(99.33)
绿豆根瘤菌
Rhizobium vignae
白城
Baicheng
NE
37 2 0.40 - 草木樨中华根瘤菌
Sinorhizobium meliloti
五河
Wuhe
N

Fig. 1

Neighbor-joining phylogenetic tree based on housekeeping gene atpD (A), glnII (B) and rpoB (C)"

Fig. 2

Neighbor-joining phylogenetic trees based on symbiotic gene nodC (A) and nifH (B)"

Table 3

The impact of Medicago sativa cultivars on the genotypes of rhizobia"

采样地
Sampling site
品种a
Cultivar
菌株数
No. of strains
BOX型b
BOX type
新乡
Xinxiang
M343 37 BOX7(4)b、BOX19(2)、BOX23(23)、BOX33(9)、BOX34(2)
M354 21 BOX7(19)、BOX33(2)
沧州
Cangzhou
中苜1号Zhongmu1 12 BOX7、BOX23(9)、BOX33、BOX35
中苜3号Zhongmu3 16 BOX19、BOX23(12)、BOX33(3)
甘农3号Gannong3 4 BOX23(4)
胶州
Jiaozhou
三得利Sandeli 12 BOX19(8)、BOX23(4)
中苜3号Zhongmu3 12 BOX19(4)、BOX23(8)
衡水
Hengshui
中苜1号Zhongmu1 31 BOX7(28)、BOX23(3)
WL363 17 BOX 19(5)、BOX23(11)、BOX33
辽阳
Liaoyang
龙牧Nongmu 13 BOX1(11)、BOX7、BOX23
WL319 21 BOX1(10)、BOX7(9)、BOX4、BOX23
[1] 徐丽君, 徐大伟, 逄焕成, 辛晓平, 金东艳, 唐雪娟, 郭明英. 中国苜蓿属植物适宜性区划. 草业科学, 2017, 11(11):2347-2358.
XU L J, XU D W, PANG H C, XIN X P, JIN D Y, TANG X J, GUO M Y. Chinese alfalfa habitat suitability regionalization. Pratacultural Science, 2017, 11(11):2347-2358. (in Chinese)
[2] 郭婷, 薛彪, 白娟, 孙启忠. 刍议中国牧草产业发展现状: 以苜蓿、燕麦为例. 草业科学, 2019, 36(5):1466-1474.
GUO T, XUE B, BAI J, SUN Q Z. Discussion of the present situation of China’s forage grass industry development: An example using alfalfa and oats. Pratacultural Science, 2019, 36(5):1466-1474. (in Chinese)
[3] 刘鹏, 田颖哲, 钟永嘉, 廖红. 酸性土壤上花生高效根瘤菌的分离及应用. 中国农业科学, 2019, 52(19):3393-3403.
LIU P, TIAN Y Z, ZHONG Y J, LIAO H. Isolation and application of effective rhizobium strains in peanut on acidic soils. Scientia Agricultura Sinica, 2019, 52(19):3393-3403. (in Chinese)
[4] 苗阳阳, 师尚礼, 康文娟. 赤霉素对根瘤菌运移、定殖及苜蓿幼苗生长的影响. 中国农业科学, 2017, 50(23):4545-4557.
MIAO Y Y, SHI S L, KANG W J. Effects of gibberellin on migration and colonization of rhizobia and seedling growth of alfalfa. Scientia Agricultura Sinica, 2017, 50(23):4545-4557. (in Chinese)
[5] 管凤贞, 邱宏端, 陈济琛, 林新坚. 根瘤菌菌剂的研究与开发现状. 生态学杂志, 2012, 31(3):755-759.
GUAN F Z, QIU H D, CHEN J C, LIN X J. Rhizobium inoculants: Research progress and development status. Chinese Journal of Ecology, 2012, 31(3):755-759. (in Chinese)
[6] 张荣娟. 中国西部苜蓿根瘤菌的生物地理分布及其抗逆机理研究[D]. 北京: 中国农业大学, 2011.
ZHANG R J. Biogeography and stress adaptation mechanisms of Sinorhizobium associated with Medicago in Western China[D]. Beijing: China Agricultural University, 2011. (in Chinese)
[7] KANG W J, SHI, S L, XU L. Diversity and symbiotic divergence of endophytic and non-endophytic rhizobia of Medicago sativa. Annals of Microbiology, 2018, 68:247-260.
doi: 10.1007/s13213-018-1333-3
[8] 张小甫. 甘肃不同生态区域苜蓿根瘤菌筛选菌株常规鉴定与分子鉴定[D]. 兰州: 甘肃农业大学, 2008.
ZHANG X F. Identification of alfalfa rhizobium strains and analysis of genetic diversity in different ecological regions in Gansu[D]. Lanzhou: Gansu Agricultural University, 2008. (in Chinese)
[9] 冯春生. 西北地区天蓝苜蓿根瘤菌系统发育研究[D]. 杨凌: 西北农林科技大学, 2008.
FENG C S. Phylogeny of rhizobia isolated from Medicago lupulina in Northwest of China[D]. Yangling: Northwest Agricultural and Forestry University, 2008. (in Chinese)
[10] 位秀丽, 付芸芸, 韦革宏. 西北部分重金属矿区天蓝苜蓿根瘤菌生理生化特性及16S rDNA PCR-RFLP分析. 干旱地区农业研究, 2009, 27(2):223-226.
WEI X L, FU Y Y, WEI G H. Physiological and biochemical characters and 16S rDNA PCR-RFLP of rhizobia isolated from Medicago lupulina in mining regions of Northwest China. Agricultural Research in the Arid Areas, 2009, 27(2):223-226. (in Chinese)
[11] 葛勇. 川西高寒地区苜蓿和无翅山黧豆根瘤菌遗传多样性及系统发育地位研究[D]. 成都: 四川农业大学, 2013.
GE Y. Genetic diversity and phylogeny of rhizobia isolated from Medicago and Lathyrus in the west plateau of Sichuan, China[D]. Chengdu: Sichuan Agricultural University, 2013. (in Chinese)
[12] STEFAN A, CAUWENBERGHE J V, ROSU C M, STEDEL C. LABROU N, FLEMETAKIS E, EFROSE R C. Genetic diversity and structure of Rhizobium leguminosarum populations associated with clover plants are influenced by local environmental variables. Systematic and Applied Microbiology, 2018, 41(3):251-259.
doi: 10.1016/j.syapm.2018.01.007
[13] WANG X L, CUI W J. FENG X Y, ZHONG Z M, LI Y, CHEN W X, CHEN W F, SHAO X M, TIAN C F. Rhizobia inhabiting nodules and rhizosphere soils of alfalfa: A strong selection of facultative microsymbionts. Soil Biology and Biochemistry, 2018, 116:340-350.
doi: 10.1016/j.soilbio.2017.10.033
[14] VERSALOVIC J, SCHNEIDER M, DE BRUIJN F J, LUPSKI J R. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods in Molecular and Cellular Biology, 1994, 5:25-40.
[15] VINUESA P, SILVA C, WERNER D, MARTINEZ-ROMERO E. Population genetics and phylogenetic inference in bacterial molecular systematics: The roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Molecular Phylogenetics and Evolution, 2005, 34(1):29-54.
doi: 10.1016/j.ympev.2004.08.020
[16] VINUESA P, ROJAS-JIMENEZ K, CONTRERAS-MOREIRA B, MAHNA S K, PRASAD B N, MOE H, SELVARAJU S B, THIERFELDER H, WERNER D. Multilocus sequence analysis for assessment of the biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybeans on the Asiatic Continent. Applied and Environmental Microbiology, 2008, 74(22):6987-6996.
doi: 10.1128/AEM.00875-08
[17] SARITA S, SHARMA P K, PRIEFER U B, PRELL J. Direct amplification of rhizobial nodC sequences from soil total DNA and comparison to nodC diversity of root nodule isolates. FEMS Microbiology Ecology, 2005, 54(1):1-11.
doi: 10.1016/j.femsec.2005.02.015
[18] YAO Y, WANG R, LU J K, SUI X H, WANG E T, CHEN W X. Genetic diversity and evolution of Bradyrhizobium populations nodulating Erythrophleum fordii, an evergreen tree indigenous to the southern subtropical region of China. Applied Environmental Microbiology, 2014, 80(19):6184-6194.
doi: 10.1128/AEM.01595-14
[19] LIU J, WANG E T, CHEN W X. Diverse rhizobia associated with woody legumes Wisteria sinensis, Cercis racemosa and Amorpha fruticosa grown in the temperate zone of China. Systematic and Applied Microbiology, 2005, 28(5):465-477.
doi: 10.1016/j.syapm.2005.02.004
[20] ZHANG X X, GUO H J, JIAO J, ZHANG P, XIONG H Y, CHEN W X, TIAN C F. Pyrosequencing of rpoB uncovers a significant biogeographical pattern of rhizobial species in soybean rhizosphere. Journal of Biogeography, 2017, 44(7):1491-1499.
doi: 10.1111/jbi.2017.44.issue-7
[21] XIONG H Y, ZHANG X X, GUO H J, JI Y Y, LI Y, WANG X L, ZHAO W, MO F Y, CHEN J C, YANG T, ZONG X X, CHEN W X, TIAN C F. The epidemicity of facultative microsymbionts in faba bean rhizosphere soils. Soil Biology and Biochemistry, 2017, 115:243-252.
doi: 10.1016/j.soilbio.2017.08.032
[22] BROWN S P, GRILLO M A, PODOWSKI J C, HEATH K D. Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula. Microbiome, 2020, 8:139.
doi: 10.1186/s40168-020-00915-9
[23] WAGNER M R, LUNDBERG D S, DEL RIO T G, TRINGE S G, DANGL J, MITCHELL-OLDS T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nature Communications, 2016, 7:12151.
doi: 10.1038/ncomms12151
[24] PORTER S S, CHANG P L, CONOW C A, DUNHAM J P, FRIESEN M L. Association mapping reveals novel serpentine adaptation gene clusters in a population of symbiotic Mesorhizobium. The ISME Journal, 2017, 11(1):248-262.
doi: 10.1038/ismej.2016.88
[25] TALEBI M B, BAHAR M, SAEIDI G, MENGONI A, BAZZICALUPO M. Diversity of Sinorhizobium strains nodulating Medicago sativa from different Iranian regions. FEMS Microbiology Letters, 2008, 288(1):40-46.
doi: 10.1111/fml.2008.288.issue-1
[26] SILVA C, KAN F L, MARTÃNEZ-ROMERO E. Population genetic structure of Sinorhizobium meliloti and S. medicae isolated from nodules of Medicago spp. in Mexico. FEMS Microbiology Ecology, 2007, 60(3):477-489.
doi: 10.1111/fem.2007.60.issue-3
[27] LING J, WANG H, WU P, LI T, TANG Y, NASEER N, ZHENG H M, MASSON-BOIVIN C, ZHONG Z T, ZHU J. Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(48):13875-13880.
[28] XIE J B, DU Z L, BAI L Q, TIAN C F, ZHANG J Z, XIE J Y, WANG T S, LIU X M, CHEN X, CHENG Q, CHEN S F, LI J L. Comparative genomic analysis of N2-fixing and non-N2-fixing Paenibacillus spp.: Organization, evolution and expression of the nitrogen fixation genes. PLoS Genetics, 2014, 10(3):e1004231.
doi: 10.1371/journal.pgen.1004231
[29] TIAN C F, ZHOU Y J, ZHANG Y M, LI Q Q, ZHANG Y Z, LI D F, WANG S, WANG J, GILBERT L B, LI R Y, CHEN W X. Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(22):8629-8634.
[30] TORO N, MARTINEZ-ABARCA F, MOLINA-SANCHEZ M D, GARCIA-RODRIGUEZ F M, NISA-MARTINEZ RAFAEL. Contribution of mobile group II introns to Sinorhizobium meliloti genome evolution. Frontier in Microbiology, 2018, 9:627.
[31] ACOSTA J L, EGUIARTE L E, SANTAMARIA R I, BUSTOS P, VINUESA P, MARTINEZ-ROMERO E, DAVILA G, GONZALEZ V. Genomic lineages of Rhizobium etli revealed by the extent of nucleotide polymorphisms and low recombination. BMC Evolutionary Biology, 2011, 11:1-13
doi: 10.1186/1471-2148-11-1
[32] EPSTEIN B, ABOU-SHANAB R A I, TAYLOR M R, GUHLIN J, BURGHARDT L T, NELSON M, SADOWSKY M J, TIFFIN P. Genome-wide association analyses in the model rhizobium Ensifer meliloti. mSphere, 2018, 3(5):e00386-e00418.
[33] WANG S W, HAO B H, LI J R, GU H L, PENG J L, XIE F L, ZHAO X Y, FRECH C, CHEN N S, MA B G, LI Y G. Whole-genome sequencing of Mesorhizobium huakuii 7653R provides molecular insights into host specificity and symbiosis island dynamics. BMC Genomics, 2014, 15(1):440.
doi: 10.1186/1471-2164-15-440
[34] REMIGI P, ZHU J, YOUNG J P W, MASSON-BOIVIN C. Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends in Microbiology, 2016, 24(1):63-75.
doi: 10.1016/j.tim.2015.10.007
[35] REJILI M, OFF K, BRACHMANN A, MARIN M. Bradyrhizobium hipponense sp. nov., isolated from Lupinus angustifolius growing in the northern region of Tunisia. International Journal of Systematic and Evolutionary Microbiology, 2020, 70(10):5539-5550.
doi: 10.1099/ijsem.0.004445
[1] KANG JunMei,ZHANG QiaoYan,JIANG Xu,WANG Zhen,ZHANG TieJun,LONG RuiCai,CUI HuiTing,YANG QingChuan. Cloning MsSQE1 from Alfalfa and Functional Analysis in Saponin Synthesis [J]. Scientia Agricultura Sinica, 2020, 53(2): 247-260.
[2] LI Qiang, HUANG YingXin, ZHONG RongZhen, SUN HaiXia, ZHOU DaoWei. Influence of Medicago sativa Proportion on Its Individual Nitrogen Fixation Efficiency and Underlying Physiological Mechanism in Legume-Grass Mixture Grassland [J]. Scientia Agricultura Sinica, 2020, 53(13): 2647-2656.
[3] Lin CHEN,RuiMing LIN,FengTao WANG,YunXing PANG,Xue LI,AiPing ZHAO,YanXia ZHANG,JinLing ZHANG,WenXing LI,SuQin HE,Jing FENG,Yun LI,CaiYi WEN,ShiChang XU. Genetic Diversity of Dactylobotrys graminicola and Its Pathogenicity to Hordeum vulgare var. nudum Seedlings [J]. Scientia Agricultura Sinica, 2020, 53(1): 213-224.
[4] CHANG JiaYing,LIU ShuSen,MA HongXia,SHI Jie,GUO Ning,ZHANG HaiJian. Genetic Diversity Analysis of Curvularia lunata in Summer Maize in Huang-Huai-Hai Region [J]. Scientia Agricultura Sinica, 2019, 52(5): 822-836.
[5] LIU HaiLu, WANG Xuan, LI HongMei, LI YanXia, XUE BoWen, MA JuKui. Molecular Identification of Pratylenchus Species in 10 Samples Collected from Wheat Field in Huanghuai Region of China [J]. Scientia Agricultura Sinica, 2018, 51(15): 2898-2912.
[6] RuiRui XU, Rui LI, XiaoFei WANG, YuJin HAO. Identification and Expression Analysis Under Abiotic Stresses of OFP Gene Family in Apple [J]. Scientia Agricultura Sinica, 2018, 51(10): 1948-1959.
[7] LI YanXing, GUO PingYi, SUN JianGuang. Isolation, Identification, Phylogeny and Growth Promoting Characteristics of Endophytic Diazotrophs from Tuber and Root Crops [J]. Scientia Agricultura Sinica, 2017, 50(1): 104-122.
[8] SHEN Lin-lin, ZOU Wen-chao, GAO Fang-luan, ZHAN Jia-sui. Strain Composition of Potato virus Y in Fujian Province Detected with the Concatenated Sequence Approach [J]. Scientia Agricultura Sinica, 2016, 49(20): 3918-3926.
[9] XU Yuan-yuan, LIN Jing, LI Xiao-gang, CHANG You-hong. Identification and Expression Analysis under Abiotic Stresses of the CBL Gene Family in Pear [J]. Scientia Agricultura Sinica, 2015, 48(4): 735-747.
[10] WANG Yu-chun, HAO Xin-yuan, HUANG Yu-ting, YUE Chuan, WANG Bo, CAO Hong-li, WANG Lu, WANG Xin-chao, YANG Ya-jun, XIAO Bin. Phylogenetic Study of Colletotrichum Species Associated with Camellia sinensis from the Major Tea Areas in China [J]. Scientia Agricultura Sinica, 2015, 48(24): 4924-4935.
[11] GAO Fang-luan, CHANG Fei, SHEN Jian-guo, XIE Lian-hui, ZHAN Jia-sui. Complete Genome Analysis of a PVYNTN-NW Recombinant Isolate from Yulin of China [J]. Scientia Agricultura Sinica, 2015, 48(2): 270-279.
[12] WANG Xuan, LE Xiu-Hu, SONG Zhi-Qiang, XIANG Gui-Lin, LIN Yu, LI Hong-Mei. Morphological and Molecular Identification of Cereal Cyst Nematodes on Wheat from Jiangsu Province of China [J]. Scientia Agricultura Sinica, 2013, 46(5): 934-942.
[13] WANG Xiao-Fei, LIU Xin, SU Ling, SUN Yong-Jiang, ZHANG Shi-Zhong, HAO Yu-Jin, YOU Chun-Xiang. Identification, Evolution and Expression Analysis of the LBD Gene Family in Tomato [J]. Scientia Agricultura Sinica, 2013, 46(12): 2501-2513.
[14] SUN Jian-Guang, LUO Qiong, GAO Miao, HU Hai-Yan, XU Jing, ZHOU Yi-Qing. Isolation and Phylogeny of Nitrogen-Fixing Endophytic Bacteria in Wheat, Rice, Maize, Chinese Cabbage and Celery [J]. Scientia Agricultura Sinica, 2012, 45(7): 1303-1317.
[15] CAO Jun-Zheng, WU Xia, LIN Sen. Identification of Fungus Lecanicillium psalliotae and Its Colonization in Different Life Stages of Meloidogyne incognita [J]. Scientia Agricultura Sinica, 2012, 45(12): 2404-2411.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!