VIGS technology: An attractive tool for functional genomics studies in legumes

Functional Plant Biology

Volumn 40, Issue 12, 2013, Pages 1234-1248

  Pflieger, Stéphanie ^a,b   Richard, Manon M S ^a   Blanchet, Sophie ^a   Meziadi, Chouaib ^a   Geffroy, Valérie ^a,c  

^a INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Fabaceae; gene functional validation; Leguminosae; post transcriptional gene silencing; RNAi; soybean.

Indexed keywords

CROP YIELD; DEFENSE MECHANISM; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; HOMOLOGY; LEGUME; RNA; VIRUS;

EID: 84887866799     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP13089     Document Type: Review

References (94)

1. Alonso JM, Ecker JR (2006) Moving forward in reverse: genetic technologies to enable genome-wide phenomic screens in Arabidopsis. Nature Reviews. Genetics 7, 524-536. doi:10.1038/nrg1893
2. Baulcombe D (2004) RNA silencing in plants. Nature 431, 356-363. doi:10.1038/nature02874
3. Benitez-Alfonso Y, Faulkner C, Ritzenthaler C, Maule AJ (2010) Plasmodesmata: gateways to local and systemic virus infection. Molecular Plant-Microbe Interactions 23, 1403-1412. doi:10.1094/MPMI-05-10-0116
4. Bennypaul HS, Mutti JS, Rustgi S, Kumar N, Okubara PA, Gill KS (2012) Virus-induced gene silencing (VIGS) of genes expressed in root, leaf, and meiotic tissues of wheat. Functional & Integrative Genomics 12, 143-156. doi:10.1007/s10142-011-0245-0
5. Berbel A, Ferrandiz C, Hecht V, Dalmais M, Lund OS, Sussmilch FC, Taylor SA, Bendahmane A, Ellis THN, Beltran JP, Weller JL, Madueno F (2012) VEGETATIVE1 is essential for development of the compound inflorescence in pea. Nature Communications 3, 797. doi:10.1038/ncomms1801
6. Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H,HayA, Johansen IE, Tsiantis M, Laufs P (2008) A conserved molecular framework for compound leaf development. Science 322, 1835-1839. doi:10.1126/science.1166168
7. Borges A, Tsai SM, Caldas DGG (2012) Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Reports 31, 827-838. doi:10.1007/s00299-011-1204-x
8. Brigneti G, Martin-Hernandez AM, Jin HL, Chen J, Baulcombe DC, Baker B, Jones JDG (2004) Virus-induced gene silencing in Solanum species. The Plant Journal 39, 264-272. doi:10.1111/j.1365-313X.2004.02122.x
9. Brunt AA, Crabtree K, Dallwitz MJ, Gibbs AJ, Watson L, Zurcher EJ (1996) 'Plant viruses online: descriptions and lists from the VIDE database.' Available at http://biology.anu.edu.au/Groups/MES/vide/[Accessed 20 August 1996]
10. Bruun-Rasmussen M, Madsen CT, Jessing S, AlbrechtsenM(2007) Stability of Barley stripe mosaic virus-induced gene silencing in barley. Molecular Plant-Microbe Interactions 20, 1323-1331. doi:10.1094/MPMI-20-11-1323
11. Burch-Smith TM, Anderson JC, Martin GB, Dinesh-Kumar SP (2004) Applications and advantages of virus-induced gene silencing for gene function studies in plants. The Plant Journal 39, 734-746. doi:10.1111/j.1365-313X.2004. 02158.x
12. Burch-Smith TM, Schiff M, Liu YL, Dinesh-Kumar SP (2006) Efficient virus-induced gene silencing in Arabidopsis. Plant Physiology 142, 21-27. doi:10.1104/pp.106.084624
13. Bustin SA (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. Journal of Molecular Endocrinology 29, 23-39. doi:10.1677/jme.0.0290023
14. Chi XY, Hu RB, Yang QL, Zhang XW, Pan LJ, Chen N, Chen MN, Yang Z, Wang T, He YA, Yu SL (2012) Validation of reference genes for gene expression studies in peanut by quantitative real-time RT-PCR. Molecular Genetics and Genomics 287, 167-176. doi:10.1007/s00438-011-0665-5
15. Constantin GD, Krath BN, MacFarlane SA, Nicolaisen M, Johansen IE, Lund OS (2004) Virus-induced gene silencing as a tool for functional genomics in a legume species. The Plant Journal 40, 622-631. doi:10.1111/j.1365-313X.2004. 02233.x
16. Constantin GD, Grønlund M, Johansen IE, Stougaard J, Lund OS (2008) Virus-induced gene silencing (VIGS) as a reverse genetic tool to study development of symbiotic root nodules. Molecular Plant-Microbe Interactions 21, 720-727. doi:10.1094/MPMI-21-6-0720
17. Csorba T, Pantaleo V, Burgyan J (2009) RNA silencing: an antiviral mechanism. In 'Advances in virus research. Vol. 75'. (Eds G Loebenstein, JP Carr) pp. 35-71. (Elsevier Academic Press: San Diego)
18. Deng XB, Elomaa P, Nguyen CX, Hytonen T, Valkonen JPT, Teeri TH(2012) Virus-induced gene silencing for Asteraceae-a reverse genetics approach for functional genomics in Gerbera hybrida. Plant Biotechnology Journal 10, 970-978. doi:10.1111/j.1467-7652.2012.00726.x
19. DeYoung BJ, InnesRW(2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nature Immunology 7, 1243-1249. doi:10.1038/ni1410
20. Díaz-Camino C, Annamalai P, Sanchez F, Kachroo A, Ghabrial SA (2011) An effective virus-based gene silencing method for functional genomics studies in common bean. Plant Methods 7, 16. doi:10.1186/1746-4811-7-16
21. Die JV, Roman B, Nadal S, Gonzalez-Verdejo CI (2010) Evaluation of candidate reference genes for expression studies in Pisum sativum under different experimental conditions. Planta 232, 145-153. doi:10.1007/s00425-010- 1158-1
22. Ding SW, VoinnetO(2007) Antiviral immunity directed by small RNAs. Cell 130, 413-426. doi:10.1016/j.cell.2007.07.039
23. Eapen S (2008) Advances in development of transgenic pulse crops. Biotechnology Advances 26, 162-168. doi:10.1016/j.biotechadv.2007. 11.001
24. Faivre-Rampant O, Gilroy EM, Hrubikova K, Hein I, Millam S, Loake GJ, Birch P, Taylor M, Lacomme C (2004) Potato virus X-induced gene silencing in leaves and tubers of potato. Plant Physiology134, 1308-1316. doi:10.1104/pp.103.037507
25. FAOSTAT (2011) http://faostat.fao.org
26. Fu DQ, Ghabrial S, KachrooA(2009)GmRAR1andGmSGT1are required for basal, R gene-mediated and systemic acquired resistance in soybean. Molecular Plant-Microbe Interactions 22, 86-95. doi:10.1094/MPMI-22-1-0086
27. Garg R, Sahoo A, Tyagi AK, Jain M (2010) Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochemical and Biophysical Research Communications 396, 283-288. doi:10.1016/j.bbrc.2010.04.079
28. Giesler LJ, Ghabrial SA, Hunt TE, Hill JH (2002) Bean pod mottle virus: a threat to US soybean production. Plant Disease 86, 1280-1289. doi:10.1094/PDIS.2002.86.12.1280
29. G?owacki S, Macioszek VK, Kononowicz AK (2011) R proteins as fundamentals of plant innate immunity. Cellular & Molecular Biology Letters 16, 1-24. doi:10.2478/s11658-010-0024-2
30. Gould B, Kramer EM (2007) Virus-induced gene silencing as a tool for functional analyses in the emerging model plant Aquilegia (columbine, Ranunculaceae). Plant Methods 3, 6. doi:10.1186/1746-4811-3-6
31. Grønlund M, Constantin G, Piednoir E, Kovacev J, Johansen IE, Lund OS (2008) Virus-induced gene silencing in Medicago truncatula and Lathyrus odorata. Virus Research 135, 345-349. doi:10.1016/j.virusres. 2008.04.005
32. Grønlund M, Olsen A, Johansen EI, Jakobsen I (2010) Protocol: using virusinduced gene silencing to study the arbuscular mycorrhizal symbiosis in Pisum sativum. Plant Methods 6, 28. doi:10.1186/1746-4811-6-28
33. Gu HC, Ghabrial SA (2005) The Bean pod mottle virus proteinase cofactor and putative helicase are symptom severity determinants. Virology 333, 271-283. doi:10.1016/j.virol.2005.01.020
34. Guenin S, Mauriat M, Pelloux J, Van Wuytswinkel O, Bellini C, Gutierrez L (2009) Normalization of qRT-PCR data: the necessity of adopting a systematic, experimental conditions-specific, validation of references. Journal of Experimental Botany 60, 487-493. doi:10.1093/jxb/ern305
35. Hernandez-Garcia CM, Martinelli AP, Bouchard RA, Finer JJ (2009) A soybean (Glycine max) polyubiquitin promoter gives strong constitutive expression in transgenic soybean. Plant Cell Reports 28, 837-849. doi:10.1007/s00299-009-0681-7
36. Holzberg S, Brosio P, Gross C, Pogue GP (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. The Plant Journal 30, 315-327. doi:10.1046/j.1365-313X.2002.01291.x
37. Hu RB, Fan CM, Li HY, Zhang QZ, Fu YF (2009) Evaluation of putative reference genes for gene expression normalization in soybean by quantitative real-time RT-PCR. BMC Molecular Biology 10, 93. doi:10.1186/1471-2199-10-93
38. Ido Y, Nakahara KS, Uyeda I (2012) White clover mosaic virus-induced gene silencing in pea. Journal of General Plant Pathology 78, 127-132. doi:10.1007/s10327-012-0360-3
39. Igarashi A, Yamagata K, Sugai T, Takahashi Y, Sugawara E, Tamura A, Yaegashi H, Yamagishi N, Takahashi T, Isogai M, Takahashi H, Yoshikawa N (2009) Apple latent spherical virus vectors for reliable and effective virus-induced gene silencing among a broad range of plants including tobacco, tomato, Arabidopsis thaliana, cucurbits, and legumes. Virology 386, 407-416. doi:10.1016/j.virol.2009.01.039
40. Juvale PS, Hewezi T, Zhang CQ, Kandoth PK, Mitchum MG, Hill JH, Whitham SA, Baum TJ (2012) Temporal and spatial Bean pod mottle virus-induced gene silencing in soybean. Molecular Plant Pathology 13, 1140-1148. doi:10.1111/j.1364-3703.2012.00808.x
41. Kachroo A, Ghabrial SA (2012) Virus-induced gene silencing in soybean. Methods in Molecular Biology (Clifton, N.J.) 894, 287-297. doi:10.1007/978-1- 61779-882-5-19
42. Kachroo A, Fu DQ, Havens W, Navarre D, Kachroo P, Ghabrial SA (2008) An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Molecular Plant-Microbe Interactions 21, 564-575. doi:10.1094/MPMI-21-5-0564
43. Kanazawa A, Inaba J, Shimura H, Otagaki S, Tsukahara S, Matsuzawa A,Kim BM, Goto K, Masuta C (2011) Virus-mediated efficient induction of epigenetic modifications of endogenous genes with phenotypic changes in plants. The Plant Journal 65, 156-168. doi:10.1111/j.1365-313X.2010. 04401.x
44. Kasai M, Kanazawa A (2012) RNA silencing as a tool to uncover gene function and engineer novel traits in soybean. Breeding Science 61, 468-479. doi:10.1270/jsbbs.61.468
45. Koganezawa H, Yanase H, Ochiai M, Sakuma T (1985) An isometric virus-like particle isolated from russet ring-diseased apple. Annals of the Phytopathological Society of Japan 51, 363.
46. Kramer EM, Holappa L, Gould B, Jaramillo MA, Setnikov D, Santiago PM (2007) Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia. The Plant Cell 19, 750-766. doi:10.1105/tpc.107.050385
47. KumagaiMH,DonsonJ, Dellacioppa G, Harvey D, Hanley K, GrillLK(1995) Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proceedings of the National Academy of Sciences of the United States of America 92, 1679-1683. doi:10.1073/pnas.92.5.1679
48. Lange M, Yellina AL, Orashakova S, Becker A (2013) Virus-induced gene silencing (VIGS) in plants: an overview of target species and the virus-derived vector systems. Methods in Molecular Biology 975, 1-14. doi:10.1007/978-1-62703- 278-0-1
49. Li Q, Fan CM, Zhang XM, Fu YF (2012) Validation of reference genes for real-time quantitative PCR normalization in soybean developmental and germinating seeds. Plant Cell Reports 31, 1789-1798. doi:10.1007/s00299-012- 1282-4
50. Lin MT, Hill JH (1983) Bean pod mottle virus-Occurrence in Nebraska and seed transmission in soybeans. Plant Disease 67, 230-233. doi:10.1094/PD-67-230
51. Liu BH, Watanabe S, Uchiyama T, Kong FJ, KanazawaA, Xia ZJ, Nagamatsu A, AraiM,YamadaT, Kitamura K, Masuta C, Harada K, AbeJ (2010) The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1. Plant Physiology 153, 198-210. doi:10.1104/pp.109.150607
52. Liu JZ, Horstman HD, Braun E, Graham MA,Zhang CQ, Navarre D, QiuWL, Lee Y, Nettleton D, Hill JH, Whitham SA (2011) Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiology 157, 1363-1378. doi:10.1104/pp.111.185686
53. Liu SM, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang CL, Jamai A, El-Mellouki T, Juvale PS, Hill J, Baum TJ, Cianzio S, Whitham SA, Korkin D, Mitchum MG,Meksem K(2012)Asoybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492, 256-260. doi:10.1038/nature11651
54. Lu R, Martin-Hernandez AM, Peart JR, Malcuit I, Baulcombe DC (2003) Virus-induced gene silencing in plants. Methods 30, 296-303. doi:10.1016/S1046-2023(03)00037-9
55. Luo T, Fan TT, Liu YN, Rothbart M, Yu J, Zhou SX, Grimm B, Luo MZ (2012) Thioredoxin redox regulates ATPase activity of magnesium chelatase CHLI subunit and modulates redox-mediated signaling in tetrapyrrole biosynthesis and homeostasis of reactive oxygen species in pea plants. Plant Physiology 159, 118-130. doi:10.1104/pp.112. 195446
56. Luo T, Luo S, Araújo WL, Schlicke H, Rothbart M, Yu J, Fan T, Fernie AR, Grimm B, Luo M (2013) Virus-induced gene silencing of pea CHLI and CHLD affects tetrapyrrole biosynthesis, chloroplast development and the primary metabolic network. Plant Physiology and Biochemistry 65, 17-26. doi:10.1016/j.plaphy.2013.01.006
57. MacFarlane SA (2010) Tobraviruses-plant pathogens and tools for biotechnology. Molecular Plant Pathology 11, 577-583. doi:10.1111/j.1364-3703. 2010.00617.x
58. Meyer JDF, Silva DCG, Yang C, Pedley KF, Zhang C, van de Mortel M, Hill JH, Shoemaker RC, Abdelnoor RV, Whitham SA, Graham MA (2009) Identification and analyses of candidate genes for Rpp4-mediated resistance to Asian soybean rust in soybean. Plant Physiology 150, 295-307. doi:10.1104/pp.108.134551
59. Molnar A, Csorba T, Lakatos L, Varallyay E, Lacomme C, Burgyan J (2005) Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. Journal of Virology 79, 7812-7818. doi:10.1128/JVI.79.12.7812-7818.2005
60. Nagamatsu A, Masuta C, Senda M, Matsuura H, Kasai A, Hong S, Kitamura K, Abe J, Kanazawa A (2007) Functional analysis of soybean genes involved in flavonoid biosynthesis by virus-induced gene silencing. Plant Biotechnology Journal 5, 778-790. doi:10.1111/j.1467-7652.2007. 00288.x
61. Nagamatsu A, Masuta C, Matsuura H, Kitamura K,AbeJ, KanazawaA(2009) Down-regulation of flavonoid 30-hydroxylase gene expression by virusinduced gene silencing in soybean reveals the presence of a threshold mRNA level associated with pigmentation in pubescence. Journal of Plant Physiology 166, 32-39. doi:10.1016/j.jplph.2008.02.002
62. Pandey AK, Yang CL, Zhang CQ, Graham MA, Horstman HD, Lee Y, Zabotina OA, Hill JH, Pedley KF, Whitham SA (2011) Functional analysis of the Asian soybean rust resistance pathway mediated by Rpp2. Molecular Plant-Microbe Interactions 24, 194-206. doi:10.1094/MPMI-08-10-0187
63. Peele C, Jordan CV, Muangsan N, Turnage M, Egelkrout E, Eagle P, Hanley-Bowdoin L, Robertson D (2001) Silencing of a meristematic gene using geminivirus-derived vectors. The Plant Journal 27, 357-366. doi:10.1046/j.1365- 313x.2001.01080.x
64. Pflieger S, Blanchet S, Camborde L, Drugeon G, Rousseau A, Noizet M, Planchais S, Jupin I (2008) Efficient virus-induced gene silencing in Arabidopsis using a 'one-step' TYMV-derived vector. The Plant Journal 56, 678-690. doi:10.1111/j.1365-313X.2008.03620.x
65. Power J (1987) Legumes: their potential role in agricultural production. American Journal of Alternative Agriculture 2, 69-73. doi:10.1017/ S0889189300001600
66. Ratcliff F, Harrison BD, Baulcombe DC (1997) A similarity between viral defense and gene silencing in plants. Science 276, 1558-1560. doi:10.1126/science.276.5318.1558
67. Robertson D (2004) VIGS vectors for gene silencing: many targets, many tools. Annual Review of Plant Biology 55, 495-519. doi:10.1146/annurev. arplant.55.031903.141803
68. Ross JP (1986) Response of early-planted and late-planted soybeans to natural infection by Bean pod mottle virus. Plant Disease 70, 222-224. doi:10.1094/PD-70-222
69. Sahu PP, Puranik S, Khan M, Prasad M (2012) Recent advances in tomato functional genomics: utilization of VIGS. Protoplasma 249, 1017-1027. doi:10.1007/s00709-012-0421-7
70. Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C, Nakayama S, Nakazaki N, Shimizu Y, Shinpo S, Takahashi C, Wada T, Yamada M, Ohmido N, Hayashi M, Fukui K, Baba T, Nakamichi T, Mori H, Tabata S (2008) Genome structure of the legume, Lotus japonicus. DNA Research 15, 227-239. doi:10.1093/dnares/dsn008
71. Schmutz J, Cannon SB, Schlueter J, Ma JX, Mitros T, Nelson W, Hyten DL, Song QJ, Thelen JJ, Cheng JL, Xu D, Hellsten U, May GD, Yu Y, Sakurai T,UmezawaT, BhattacharyyaMK,Sandhu D, ValliyodanB, Lindquist E, Peto M, Grant D, Shu SQ, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du JC, Tian ZX, Zhu LC, Gill N, Joshi T, Libault M, Sethuraman A, ZhangXC, Shinozaki K, NguyenHT,WingRA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463, 178-183. doi:10.1038/nature08670
72. Scofield SR, Nelson RS (2009) Resources for virus-induced gene silencing in the grasses. Plant Physiology 149, 152-157. doi:10.1104/pp.108.128702
73. Senthil-Kumar M, Mysore KS (2011a) New dimensions for VIGS in plant functional genomics. Trends in Plant Science 16, 656-665. doi:10.1016/j.tplants. 2011.08.006
74. Senthil-Kumar M, Mysore KS (2011b) Virus-induced gene silencing can persist for more than 2 years and also be transmitted to progeny seedlings in Nicotiana benthamiana and tomato. Plant Biotechnology Journal 9, 797-806. doi:10.1111/j.1467-7652.2011.00589.x
75. Singh AK, Fu DQ, El-Habbak M, Navarre D, Ghabrial S, Kachroo A (2011) Silencing genes encoding omega-3 fatty acid desaturase alters seed size and accumulation of Bean pod mottle virus in soybean. Molecular Plant-Microbe Interactions 24, 506-515. doi:10.1094/MPMI-09-10-0201
76. Terpolilli JJ, Hood GA, Poole PS (2012) What determines the efficiency of N2-fixing Rhizobium-legume symbioses? Advances in Microbial Physiology 60, 325-389. doi:10.1016/B978-0-12-398264-3.00005-X
77. Thomas CL, Jones L, Baulcombe DC, Maule AJ (2001) Size constraints for targeting post-transcriptional gene silencing and for RNA-directed methylation in Nicotiana benthamiana using a Potato virus X vector. The Plant Journal 25, 417-425. doi:10.1046/j.1365-313x.2001.00976.x
78. Turnage MA, Muangsan N, Peele CG, Robertson D (2002) Geminivirusbased vectors for gene silencing in Arabidopsis. The Plant Journal 30, 107-114. doi:10.1046/j.1365-313X.2002.01261.x
79. Ueki S, CitovskyV (2011) To gate, or not to gate: regulatory mechanisms for intercellular protein transport and virus movement in plants. Molecular Plant 4, 782-793. doi:10.1093/mp/ssr060
80. Unver T, Budak H (2009) Conserved microRNAs and their targets in model grass species Brachypodium distachyon. Planta 230, 659-669. doi:10.1007/s00425- 009-0974-7
81. Várallyay E, Lichner Z, Sáfrány J, Havelda Z, Salamon P, Bisztray G, Burgyán J (2010) Development of a virus induced gene silencing vector from a legumes infecting tobamovirus. Acta Biologica Hungarica 61, 457-469. doi:10.1556/ABiol.61.2010.4.9
82. Varshney RK, Chen WB, Li YP, Bharti AK, Saxena RK, Schlueter JA, Donoghue MTA, Azam S, Fan GY, Whaley AM, Farmer AD, Sheridan J, Iwata A, Tuteja R, Penmetsa RV, Wu W, Upadhyaya HD, Yang SP, Shah T, Saxena KB, Michael T, McCombie WR, Yang BC, Zhang GY, Yang HM, Wang J, Spillane C, Cook DR, May GD, Xu X, Jackson SA (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nature Biotechnology 30, 83-89. doi:10.1038/nbt.2022
83. Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG, Cannon S, Baek J, Rosen BD, Tar'an B, Millan T, Zhang X, Ramsay LD, Iwata A, Wang Y, Nelson W, Farmer AD, Gaur PM, Soderlund C, Penmetsa RV, Xu C, Bharti AK, He W, Winter P, Zhao S, Hane JK, Carrasquilla-Garcia N, Condie JA, Upadhyaya HD, Luo MC, Thudi M, Gowda CL, Singh NP, Lichtenzveig J, Gali KK, Rubio J, Nadarajan N, Dolezel J, Bansal KC, Xu X, Edwards D, Zhang G, Kahl G, Gil J, Singh KB, Datta SK, Jackson SA, Wang J, Cook DR (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nature Biotechnology 31, 240-246. doi:10.1038/nbt.2491
84. Vuorinen AL, Kelloniemi J, Valkonen JPT (2011) Why do viruses need phloem for systemic invasion of plants? Plant Science 181, 355-363. doi:10.1016/j.plantsci.2011.06.008
85. Wang DW, Maule AJ (1997) Contrasting patterns in the spread of two seed-borne viruses in pea embryos. The Plant Journal 11, 1333-1340. doi:10.1046/j.1365-313X.1997.11061333.x
86. Wang Z, Luo YH, Li X, Wang LP,Xu SL, Yang J, Weng L, Sato SS, Tabata S, Ambrose M, Rameau C, Feng XZ, Hu XH, Luo D (2008) Genetic control of floral zygomorphy in pea (Pisum sativum L.). Proceedings of the National Academy of Sciences of the United States of America 105, 10414-10419. doi:10.1073/pnas. 0803291105
87. Yamagishi N, Yoshikawa N (2009) Virus-induced gene silencing in soybean seeds and the emergence stage of soybean plants with Apple latent spherical virus vectors. Plant Molecular Biology 71, 15-24. doi:10.1007/s11103-009-9505-y
88. Young ND, Debelle F, Oldroyd GED, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KFX, Gouzy J, Schoof H, et al. (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480, 520-524.
89. Zaumeyer WJ, Thomas HR (1948) Pod mottle, a virus disease of beans. Journal of Agricultural Research 77, 81-96.
90. Zhang C, Ghabrial SA (2006) Development of Bean pod mottle virus-based vectors for stable protein expression and sequence-specific virus-induced gene silencing in soybean. Virology 344, 401-411. doi:10.1016/j.virol. 2005.08.046
91. Zhang C, Yang CL, Whitham SA, Hill JH (2009) Development and use of an efficient DNA-based viral gene silencing vector for soybean. Molecular Plant-Microbe Interactions 22, 123-131. doi:10.1094/MPMI-22-2-0123
92. ZhangCQ, Bradshaw JD, WhithamSA, HillJH (2010) The development of an efficient multipurpose Bean pod mottle virus viral vector set for foreign gene expression and RNA silencing. Plant Physiology 153, 52-65. doi:10.1104/pp.109. 151639
93. Zhang CQ, Grosic S, Whitham SA, Hill JH (2012) The requirement of multiple defense genes in soybean Rsv1-mediated extreme resistance to Soybean mosaic virus. Molecular Plant-Microbe Interactions 25, 1307-1313. doi:10.1094/MPMI-02-12-0046-R
94. Zhang C, Whitham SA, Hill JH (2013) Virus-induced gene silencing in soybean and common bean. Methods in Molecular Biology (Clifton, N.J.) 975, 149-156. doi:10.1007/978-1-62703-278-0-11