1932

Abstract

Understanding the coevolutionary history of plants, pathogens, and disease resistance is vital for plant pathology. Here, I review Francis O. Holmes's work with tobacco mosaic virus (TMV) framed by the foundational work of Nikolai Vavilov on the geographic centers of origin of plants and crop wild relatives (CWRs) and T. Harper Goodspeed's taxonomy of the genus . Holmes developed a hypothesis that the origin of host resistance to viruses was due to coevolution of both at a geographic center. In the 1950s, Holmes proved that genetic resistance to TMV, especially dominant -genes, was centered in South America for and other solanaceous plants, including , potato, and tomato. One seeming exception was eggplant (). Not until the acceptance of plate tectonics in the 1960s and recent advances in evolutionary taxonomy did it become evident that northeast Africa was the home of eggplant CWRs, far from Holmes's geographic center for TMV–-gene coevolution. Unbeknownst to most plant pathologists, Holmes's ideas predated those of H.H. Flor, including experimental proof of the gene-for-gene interaction, identification of -genes, and deployment of dominant host genes to protect crop plants from virus-associated yield losses.

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2023-09-05
2024-04-27
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Literature Cited

  1. 1.
    Ala-Poikela M, Goytia E, Haikonen T, Rajamäki M-L, Valkonen Jari PT 2011. Helper component proteinase of the genus Potyvirus is an interaction partner of translation initiation factors eIF(iso)4E and eIF4E and contains a 4E binding motif. J. Virol. 85:6784–94
    [Google Scholar]
  2. 2.
    Allard HA. 1914. The mosaic disease of tobacco. Bur. Plant Ind. Bull. 40 US Dep. Agric. Washington, DC:
  3. 3.
    Andolfo G, Di Donato A, Chiaiese P, De Natale A, Pollio A et al. 2019. Alien domains shaped the modular structure of plant NLR proteins. Genome Biol. Evol. 11:3466–77
    [Google Scholar]
  4. 4.
    Aubriot X, Knapp S, Syfert MM, Poczai P, Buerki S. 2018. Shedding new light on the origin and spread of the brinjal eggplant (Solanummelongena L.) and its wild relatives. Am. J. Bot. 105:1175–87
    [Google Scholar]
  5. 5.
    Aubriot X, Singh P, Knapp S. 2016. Tropical Asian species show that the Old World clade of ‘spiny solanums’ (Solanum subgenus Leptostemonumpro parte: Solanaceae) is not monophyletic. Bot. J. Linn. Soc. 181:199–223
    [Google Scholar]
  6. 6.
    Balaji B, Cawly J, Angel C, Zhang Z, Palanichelvam K et al. 2007. Silencing of the N family of resistance genes in Nicotianaedwardsonii compromises the hypersensitive response to Tombusviruses. Mol. Plant-Microbe Interact. 20:1262–70
    [Google Scholar]
  7. 7.
    Barragan AC, Weigel D. 2021. Plant NLR diversity: the known unknowns of pan-NLRomes. Plant Cell 33:814–31
    [Google Scholar]
  8. 8.
    Botermans M, de Koning PPM, Oplaat C, Fowkes A, McGreig S et al. 2023. Tomato brown rugose fruit virus Nextstrain build version 3: rise of a novel clade. PhytoFrontiers. https://doi.org/10.1094/PHYTOFR-09-22-0090-A
    [Crossref] [Google Scholar]
  9. 9.
    Brakke MK. 1984. Mutations, the aberrant ratio phenomenon, and virus infection of maize. Annu. Rev. Phytopathol. 22:77–94
    [Google Scholar]
  10. 10.
    Brakke MK, Samson RG, Compton WA. 1981. Recessive alleles found at R and C loci in maize stocks showing aberrant ratio at the A locus. Genetics 99:481–85
    [Google Scholar]
  11. 11.
    Caruso AG, Bertacca S, Parrella G, Rizzo R, Davino S, Panno S. 2022. Tomato brown rugose fruit virus: a pathogen that is changing the tomato production worldwide. Ann. Appl. Biol. 181:258–74
    [Google Scholar]
  12. 12.
    Clausen RE, Goodspeed TH. 1925. Interspecific hybridization in Nicotiana. II. A tetraploid glutinosa-tabacum hybrid, an experimental verification of Winge's hypothesis. Genetics 10:278–84
    [Google Scholar]
  13. 13.
    Cohen BM. 1991. Nikolai Ivanovich Vavilov: the explorer and plant collector. Econ. Bot. 45:38–46
    [Google Scholar]
  14. 14.
    Creager ANH. 2002. The Life of a Virus: Tobacco Mosaic Virus as an Experimental Model, 19301965 Chicago: Univ. Chicago Press
    [Google Scholar]
  15. 15.
    Creager ANH. 2022. Tobacco mosaic virus and the history of molecular biology. Annu. Rev. Virol. 9:39–55
    [Google Scholar]
  16. 16.
    Curry HA. 2019. Why save a seed?. Isis 110:337–40
    [Google Scholar]
  17. 17.
    Dardick CD, Culver JN. 1997. Tobamovirus coat proteins: elicitors of the hypersensitive response in Solanummelongena (eggplant). Mol. Plant-Microbe Interact. 10:776–78
    [Google Scholar]
  18. 18.
    Delaux P-M, Schornack S. 2021. Plant evolution driven by interactions with symbiotic and pathogenic microbes. Science 371:eaba6605
    [Google Scholar]
  19. 19.
    Dolja VV, Krupovic M, Koonin EV. 2020. Deep roots and splendid boughs of the global plant virome. Annu. Rev. Phytopathol. 58:23–53
    [Google Scholar]
  20. 20.
    Domingo E, García-Crespo C, Perales C. 2021. Historical perspective on the discovery of the quasispecies concept. Annu. Rev. Virol. 8:51–72
    [Google Scholar]
  21. 21.
    Elena SF. 2017. Local adaptation of plant viruses: lessons from experimental evolution. Mol. Ecol. 26:1711–19
    [Google Scholar]
  22. 22.
    Fraile A, Hily J-M, Pagán I, Pacios LF, García-Arenal F. 2014. Host resistance selects for traits unrelated to resistance-breaking that affect fitness in a plant virus. Mol. Biol. Evol. 31:928–39
    [Google Scholar]
  23. 23.
    Fraser RSS, Gerwitz A 1987. The genetics of resistance and virulence in plant virus disease. Genetics and Plant Pathogenesis PR Day, GJ Jellis 33–44. Oxford, UK: Blackwell
    [Google Scholar]
  24. 24.
    Fukuhara T, Tabara M, Koiwa H, Takahashi H. 2020. Effect of asymptomatic infection with southern tomato virus on tomato plants. Arch. Virol. 165:11–20
    [Google Scholar]
  25. 25.
    Fullilove C. 2017. The Profit of the Earth: The Global Seeds of American Agriculture Chicago: Univ. Chicago Press
    [Google Scholar]
  26. 26.
    Gambino G, Cuozzo D, Fasoli M, Pagliarani C, Vitali M et al. 2012. Co-evolution between Grapevine rupestris stem pitting-associated virus and Vitisvinifera L. leads to decreased defence responses and increased transcription of genes related to photosynthesis. J. Exp. Bot. 63:5919–33
    [Google Scholar]
  27. 27.
    Gao Y, Wang W, Zhang T, Gong Z, Zhao H, Han G-Z. 2018. Out of water: the origin and early diversification of plant R-genes. Plant Physiol 177:82–89
    [Google Scholar]
  28. 28.
    Gibbs A. 1980. A plant virus that partially protects its wild legume host against herbivores. Intervirology 13:42–47
    [Google Scholar]
  29. 29.
    Gibbs AJ, Wood J, Garcia-Arenal F, Ohshima K, Armstrong JS. 2015. Tobamoviruses have probably co-diverged with their eudicotyledonous hosts for at least 110 million years. Virus Evol 1:vev019
    [Google Scholar]
  30. 30.
    Goodspeed TH. 1945. Cytotaxonomy of Nicotiana. Bot. Rev. 11:533–92
    [Google Scholar]
  31. 31.
    Goodspeed TH. 1947. On the evolution of the genus Nicotiana. PNAS 33:158–71
    [Google Scholar]
  32. 32.
    Goodspeed TH. 1954. The Genus Nicotiana: Origins, Relationships and Evolution of its Species in the Light of Their Distribution, Morphology and Cytogenetics Waltham, MA: Chronica Botanica
    [Google Scholar]
  33. 33.
    Grant TJ. 1934. The host range and behavior of the ordinary tobacco-mosaic virus. Phytopathology 24:311–36
    [Google Scholar]
  34. 34.
    Greene MT. 2015. Alfred Wegener: Science, Exploration, and the Theory of Continental Drift Baltimore: Johns Hopkins Univ. Press
    [Google Scholar]
  35. 35.
    Hak H, Spiegelman Z. 2021. The Tomato brown rugose fruit virus movement protein overcomes Tm-22 resistance in tomato while attenuating viral transport. Mol. Plant-Microbe Interact. 34:1024–32
    [Google Scholar]
  36. 36.
    Hawkes JG. 1988. The evolution of cultivated potatoes and their tuber-bearing wild relatives. Die Kulturpflanze 36:189–208
    [Google Scholar]
  37. 37.
    Holmes FO. 1932. Symptoms of tobacco mosaic disease. Contrib. Boyce Thompson Inst 4:323–57
    [Google Scholar]
  38. 38.
    Holmes FO. 1934. A masked strain of tobacco-mosaic virus. Phytopathology 24:845–73
    [Google Scholar]
  39. 39.
    Holmes FO. 1934. Inheritance of ability to localize tobacco-mosaic virus. Phytopathology 24:984–1002
    [Google Scholar]
  40. 40.
    Holmes FO. 1936. Interspecific transfer of a gene governing type of response to tobacco-mosaic infection. Phytopathology 26:1007–14
    [Google Scholar]
  41. 41.
    Holmes FO. 1937. Hereditary factors affecting tobacco-mosaic disease in solanaceous plants. Phytopathology 27:131–32
    [Google Scholar]
  42. 42.
    Holmes FO. 1937. Inheritance of resistance to tobacco-mosaic disease in the pepper. Phytopathology 27:637–42
    [Google Scholar]
  43. 43.
    Holmes FO. 1938. Inheritance of resistance to tobacco-mosaic disease in Browallia. Phytopathology 28:363–69
    [Google Scholar]
  44. 44.
    Holmes FO. 1938. Inheritance of resistance to tobacco-mosaic disease in tobacco. Phytopathology 28:553–61
    [Google Scholar]
  45. 45.
    Holmes FO. 1938. Taxonomic relationships of plants susceptible to infection by tobacco-mosaic virus. Phytopathology 28:58–66
    [Google Scholar]
  46. 46.
    Holmes FO. 1939. The Chilean tomato, Lycopersiconchilense, as a possible source of disease resistance. Phytopathology 29:215–16
    [Google Scholar]
  47. 47.
    Holmes FO. 1942. Quantitative measurement of a strain of tobacco-etch virus. Phytopathology 32:1058–67
    [Google Scholar]
  48. 48.
    Holmes FO. 1946. A comparison of the experimental host ranges of tobacco-etch and tobacco-mosaic viruses. Phytopathology 36:643–59
    [Google Scholar]
  49. 49.
    Holmes FO. 1951. Indications of a New-World origin of tobacco-mosaic virus. Phytopathology 41:341–49
    [Google Scholar]
  50. 50.
    Holmes FO. 1952. Geographical isolation of some viral diseases. Plant Dis. Rep. 211:Suppl.37–42
    [Google Scholar]
  51. 51.
    Holmes FO. 1954. Inheritance of resistance to viral diseases in plants. Adv. Virus Res. 2:1–30
    [Google Scholar]
  52. 52.
    Holmes FO. 1955. Additive resistances to specific viral diseases in plants. Ann. Appl. Biol. 42:129–39
    [Google Scholar]
  53. 53.
    Holmes FO. 1968. Trends in the development of plant virology. Annu. Rev. Phytopathol. 6:41–62
    [Google Scholar]
  54. 54.
    Ishibashi K, Mawatari N, Miyashita S, Kishino H, Meshi T, Ishikawa M. 2012. Coevolution and hierarchical interactions of Tomato mosaic virus and the resistance gene Tm-1. PLOS Pathog 8:e1002975
    [Google Scholar]
  55. 55.
    Ishibashi K, Meshi T, Ishikawa M. 2011. Gaining replicability in a nonhost compromises the silencing suppression activity of Tobacco mild green mosaic virus in a host. J. Virol. 85:1893–95
    [Google Scholar]
  56. 56.
    Jayasinghe WH, Kim H, Nakada Y, Masuta C. 2021. A plant virus satellite RNA directly accelerates wing formation in its insect vector for spread. Nat. Commun. 12:7087
    [Google Scholar]
  57. 57.
    Jin H, Du Z, Zhang Y, Antal J, Xia Z et al. 2020. A distinct class of plant and animal viral proteins that disrupt mitosis by directly interrupting the mitotic entry switch Wee1-Cdc25-Cdk1. Sci. Adv. 6:eaba3418
    [Google Scholar]
  58. 58.
    Johnson J, Grant TJ. 1932. The properties of plant viruses from different host species. Phytopathology 23:741–57
    [Google Scholar]
  59. 59.
    Karasov TL, Horton MW, Bergelson J. 2014. Genomic variability as a driver of plant–pathogen coevolution?. Curr. Opin. Plant Biol. 18:24–30
    [Google Scholar]
  60. 60.
    Kim S, Park J, Yeom S-I, Kim Y-M, Seo E et al. 2017. New reference genome sequences of hot pepper reveal the massive evolution of plant disease-resistance genes by retroduplication. Genome Biol 18:210
    [Google Scholar]
  61. 61.
    Knapp S, Vorontsova MS, Prohens J. 2013. Wild relatives of the eggplant (Solanummelongena L.: Solanaceae): new understanding of species names in a complex group. PLOS ONE 8:e57039
    [Google Scholar]
  62. 62.
    Kondo H, Botella L, Suzuki N. 2022. Mycovirus diversity and evolution revealed/inferred from recent studies. Annu. Rev. Phytopathol. 60:307–36
    [Google Scholar]
  63. 63.
    Koonin EV, Dolja VV, Krupovic M, Kuhn JH. 2021. Viruses defined by the position of the virosphere within the replicator space. Microbiol. Mol. Biol. Rev. 85:e00193–20
    [Google Scholar]
  64. 64.
    Leach JG. 1935. Insects in relation to plant diseases. Bot. Rev. 1:448–66
    [Google Scholar]
  65. 65.
    Leach JG. 1940. Insect Transmission of Plant Diseases New York: McGraw-Hill
  66. 66.
    Lefeuvre P, Martin DP, Elena SF, Shepherd DN, Roumagnac P, Varsani A. 2019. Evolution and ecology of plant viruses. Nat. Rev. Microbiol. 17:632–44
    [Google Scholar]
  67. 67.
    Leppik EE. 1969. The life and work of N. I. Vavilov. Econ. Bot. 23:128–32
    [Google Scholar]
  68. 68.
    Leppik EE. 1970. Gene centers of plants as sources of disease resistance. Annu. Rev. Phytopathol. 8:323–44
    [Google Scholar]
  69. 69.
    López-Berenguer C, Donaire L, González-Ibeas D, Gómez-Aix C, Truniger V et al. 2020. Virus-infected melon plants emit volatiles that induce gene deregulation in neighboring healthy plants. Phytopathology 111:862–69
    [Google Scholar]
  70. 70.
    McKinney HH. 1929. Mosaic diseases in the Canary Islands, West Africa, and Gibraltar. J. Agric. Res. 39:557–78
    [Google Scholar]
  71. 71.
    McKinney HH. 1935. Evidence of virus mutation in common mosaic virus of tobacco. J. Agric. Res. 51:951–81
    [Google Scholar]
  72. 72.
    McKinney HH. 1937. Virus mutation and the gene concept. J. Hered. 28:51–57
    [Google Scholar]
  73. 73.
    Mez C, Ziegenspeck H. 1926. Der Königsberger serodiagnostische Stammbaum. Bot. Arch. 13:483–86
    [Google Scholar]
  74. 74.
    Nabhan GP. 2008. Where Our Food Comes From: Retracing Nikolay Vavilov's Quest to End Famine Washington, DC: Island Press
    [Google Scholar]
  75. 75.
    Oreskes N. 1999. The Rejection of Continental Drift: Theory and Method in American Earth Science Cary, NC: Oxford Univ. Press
    [Google Scholar]
  76. 76.
    Ortiz D, Dodds PN. 2018. Plant NLR origins traced back to green algae. Trends Plant Sci 23:651–54
    [Google Scholar]
  77. 77.
    Peters JS, Aguirre BA, DiPaola A, Power AG. 2022. Ecology of yellow dwarf viruses in crops and grasslands: interactions in the context of climate change. Annu. Rev. Phytopathol. 60:283–305
    [Google Scholar]
  78. 78.
    Price WC. 1930. Local lesions on bean leaves inoculated with tobacco mosaic virus. Am. J. Bot. 17:694–702
    [Google Scholar]
  79. 79.
    Rivarez MPS, Pecman A, Bačnik K, Maksimović O, Vučurović A et al. 2023. In-depth study of tomato and weed viromes reveals undiscovered plant virus diversity in an agroecosystem. Microbiome 1160
  80. 80.
    Salem N, Mansour A, Ciuffo M, Falk BW, Turina M. 2016. A new tobamovirus infecting tomato crops in Jordan. Arch. Virol. 161:503–6
    [Google Scholar]
  81. 81.
    Salem NM, Sulaiman A, Samarah N, Turina M, Vallino M. 2021. Localization and mechanical transmission of tomato brown rugose fruit virus in tomato seeds. Plant Dis 106:275–81
    [Google Scholar]
  82. 82.
    Samson RG, Brakke MK, Compton WA. 1979. Evidence for gene inactivation in the virus-induced aberrant ratio phenomenon in maize. Genetics 92:1231–39
    [Google Scholar]
  83. 83.
    Sankaran N. 2018. On the historical significance of Beijerinck and his contagiumvivumfluidum for modern virology. Hist. Philos. Life Sci. 40:41
    [Google Scholar]
  84. 84.
    Scholthof K-BG. 2004. Tobacco mosaic virus: a model system for plant biology. Annu. Rev. Phytopathol. 42:13–34
    [Google Scholar]
  85. 85.
    Scholthof K-BG. 2007. The disease triangle: pathogens, the environment and society. Nat. Rev. Microbiol. 5:152–56
    [Google Scholar]
  86. 86.
    Scholthof K-BG. 2011. Taking some of the mystery out of host:virus interactions. PLOS Pathog 7:e1002033
    [Google Scholar]
  87. 87.
    Scholthof K-BG. 2014. Making a virus visible: Francis O. Holmes and a biological assay for Tobacco mosaic virus. J. Hist. Biol. 47:107–45
    [Google Scholar]
  88. 88.
    Scholthof K-BG. 2015. Finding our roots and celebrating our shoots: plant virology in Virology, 1955–1964. Virology 478–480:345–55
    [Google Scholar]
  89. 89.
    Scholthof K-BG. 2016. Spicing up the N gene: F. O. Holmes and tobacco mosaic virus resistance in Capsicum and Nicotiana plants. Phytopathology 107:148–57
    [Google Scholar]
  90. 90.
    Scholthof K-BG, Jackson AO, Van Etten JE. 2008. Myron Kendall Brakke: 1921 to; 2007. Phytopathology 98:1056–59
    [Google Scholar]
  91. 91.
    Scholthof K-BG, Peterson PD. 2006. The role of Helen Purdy Beale in the early development of plant serology and virology. Adv. Appl. Microbiol. 59:221–41
    [Google Scholar]
  92. 92.
    Scholthof K-BG, Shaw JG, Zaitlin M, eds. 1999. Tobacco Mosaic Virus: One Hundred Years of Contributions to Virology St. Paul, MN: APS Press
    [Google Scholar]
  93. 93.
    Scholthof K-BG, Washington LJ, DeMell A, Mendoza MR, Cody WB. 2022. Practicing virology: making and knowing a mid-twentieth century experiment with Tobacco mosaic virus. Hist. Philos. Life Sci. 44:3
    [Google Scholar]
  94. 94.
    Shao Z-Q, Xue J-Y, Wang Q, Wang B, Chen J-Q. 2019. Revisiting the origin of plant NBS-LRR genes. Trends Plant Sci 24:9–12
    [Google Scholar]
  95. 95.
    Shimura H, Pantaleo V, Ishihara T, Myojo N, Burgyán J, Masuta C. 2011. A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLOS Pathog. 7:5e1002021
    [Google Scholar]
  96. 96.
    Smith NA, Eamens AL, Wang M-B. 2011. Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLOS Pathog 7:e1002022
    [Google Scholar]
  97. 97.
    van Helvoort T. 1991. What is a virus? The case of tobacco mosaic disease. Stud. Hist. Philos. Sci. 22:557–88
    [Google Scholar]
  98. 98.
    van Helvoort T, Sankaran N. 2019. How seeing became knowing: the role of the electron microscope in shaping the modern definition of viruses. J. Hist. Biol. 52:125–60
    [Google Scholar]
  99. 99.
    Vavilov NI. 1932. The process of evolution in cultivated plants. Proceedings of the Sixth International Congress of Genetics, Ithaca, NY, USA331–42. Menasha, WI: Brooklyn Bot. Gard.
    [Google Scholar]
  100. 100.
    Vavilov NI. 1949/1950. The Origin, Variation, Immunity and Breeding of Cultivated Plants Waltham, MA: Chronica Botanica Co.
    [Google Scholar]
  101. 101.
    Vlok M, Gibbs AJ, Suttle CA 2019. Metagenomes of a freshwater Charavirus from British Columbia provide a window into ancient lineages of viruses. Viruses 11:299
    [Google Scholar]
  102. 102.
    Yan Z-Y, Ma H-Y, Wang L, Tettey C, Zhao M-S et al. 2021. Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the Tm-22 resistance gene. Mol. Plant Pathol. 22:1347–57
    [Google Scholar]
  103. 103.
    Zafirov D, Giovinazzo N, Bastet A, Gallois J-L. 2021. When a knockout is an Achilles’ heel: resistance to one potyvirus species triggers hypersusceptibility to another one in Arabidopsis thaliana. Mol. Plant Pathol. 22:334–47
    [Google Scholar]
  104. 104.
    Zhang S, Griffiths JS, Marchand G, Bernards MA, Wang A. 2022. Tomato brown rugose fruit virus: an emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide. Mol. Plant Pathol. 23:1262–77
    [Google Scholar]
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