What proteomics can reveal about plant–virus interactions? Photosynthesis-related proteins on the spotlight

  • Pedro F. N. Souza
  • Hernan Garcia-Ruiz
  • Fabricio E. L. CarvalhoEmail author


Plant viruses are responsible for losses in worldwide production of numerous economically important food and fuel crops. As obligate cellular parasites with very small genomes, viruses rely on their hosts for replication, assembly, intra- and intercellular movement, and attraction of vectors for dispersal. Chloroplasts are photosynthesis and are the site of replication for several viruses. When viruses replicate in chloroplasts, photosynthesis, an essential process in plant physiology, is inhibited. The mechanisms underlying molecular and biochemical changes during compatible and incompatible plants–virus interactions, are only beginning to be elucidated, including changes in proteomic profiles induced by virus infections. In this review, we highlight the importance of proteomic studies to understand plant–virus interactions, especially emphasizing the changes in photosynthesis-related protein accumulation. We focus on: (a) chloroplast proteins that differentially accumulate during viral infection; (b) the significance with respect to chloroplast-virus interaction; and (c) alterations in plant’s energetic metabolism and the subsequently the plant defense mechanisms to overcome viral infection.


Plant–virus interactions Virus replication in chloroplasts Proteomics Photosynthesis Proteome 



This study was supported by the following Brazilian institutions: CNPq (National Council for Scientific and Technological Development. Process Numbers: 308107/2013-6 and 306202/2017-4); CAPES (Coordination of Improvement of Higher Education. Toxinology Project, Process Number: 431511/2016-0) and Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP). FELC is supported by FUNCAP/CAPES (Bolsista CAPES/BRASIL – Proc. 88887.162856/2018-00). Research at the Garcia-Ruiz lab is supported by NIH grant R01GM120108 to Hernan Garcia-Ruiz and by the Nebraska Agricultural Experiment Station with funding from the Hatch Act (Accession Number 1007272) through the USDA National Institute of Food and Agriculture.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Acosta-Leal R, Duffy S, Xiong Z, Hammond R, Elena SF (2011) Advances in plant virus evolution: translating evolutionary insights into better disease management. Phytopathology 101:1136–1148CrossRefPubMedGoogle Scholar
  2. Ahn TK, Avenson TJ, Ballottari M, Cheng Y-C, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797CrossRefPubMedGoogle Scholar
  3. Alexander MM, Cilia M (2016) A molecular tug-of-war: global plant proteome changes during viral infection. Curr Plant Biol 5:13–24CrossRefGoogle Scholar
  4. Andralojc PJ, Carmo-Silva E, Degen GE, Parry MAJ (2018) Increasing metabolic potential: C-fixation. Essays Biochem 62:109–118CrossRefPubMedGoogle Scholar
  5. Aro EM, McCaffery S, Anderson JM (1993) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 103:835–843CrossRefPubMedPubMedCentralGoogle Scholar
  6. Balasubramaniam M, Kim B-S, Hutchens-Williams HM, Loesch-Fries LS (2014) The photosystem II oxygen-evolving complex protein PsbP interacts with the coat protein of Alfalfa mosaic virus and inhibits virus replication. Mol Plant Microbe Interact 27:1107–1118CrossRefPubMedGoogle Scholar
  7. Baltimore D (1971) Expression of animal virus genomes. Bacteriol Rev 35:235–241PubMedPubMedCentralGoogle Scholar
  8. Beltran PMJ, Federspiel JD, Sheng X, Cristea IM (2017) Proteomics and integrative omic approaches for understanding host–pathogen interactions and infectious diseases. Mol Syst Biol 13:922CrossRefGoogle Scholar
  9. Bhattacharyya D, Chakraborty S (2018) Chloroplast: the Trojan horse in plant–virus interaction. Mol Plant Pathol 19:504–518CrossRefPubMedGoogle Scholar
  10. Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503CrossRefPubMedGoogle Scholar
  11. Bolton MD (2009) Primary metabolism and plant defense—fuel for the fire. Mol Plant Microbe Interact 22:487–497CrossRefPubMedGoogle Scholar
  12. Bricker TM, Frankel LK (2011) Auxiliary functions of the PsbO, PsbP and PsbQ proteins of higher plant photosystem II: a critical analysis. J Photochem Photobiol B Biol 104:165–178CrossRefGoogle Scholar
  13. Busch FA, Sage RF, Farquhar GD (2018) Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nat Plants 4:46–54CrossRefPubMedGoogle Scholar
  14. Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar S (2008) Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132:449–462CrossRefPubMedPubMedCentralGoogle Scholar
  15. Carmo LS, Murad AM, Resende RO, Boiteux LS, Ribeiro SG, Jorrín-Novo JV, Mehta A (2017) Plant responses to tomato chlorotic mottle virus: proteomic view of the resistance mechanisms to bipartite begomovirus in tomato. J Proteom 151:284–292CrossRefGoogle Scholar
  16. Carmo-Silva AE, Salvucci ME (2011) The activity of Rubisco’s molecular chaperone, Rubisco activase, in leaf extracts. Photosynth Res 108:143–155CrossRefPubMedGoogle Scholar
  17. Cerna H, Černý M, Habánová H, Šafářová D, Abushamsiya K, Navrátil M, Brzobohatý B (2017) Proteomics offers insight to the mechanism behind Pisum sativum L. response to pea seed-borne mosaic virus (PSbMV). J Proteom 153:78–88CrossRefGoogle Scholar
  18. Chaerle L, Van Caeneghem W, Messens E, Lambers H, Van Montagu M, Van Der Straeten D (1999) Presymptomatic visualization of plant–virus interactions by thermography. Nat Biotechnol 17:813–816CrossRefPubMedGoogle Scholar
  19. Cheng S-F, Huang Y-P, Chen L-H, Hsu Y-H, Tsai C-H (2013) Chloroplast phosphoglycerate kinase is involved in the targeting of Bamboo mosaic virus to chloroplasts in Nicotiana benthamiana plants. Plant Physiol 163:1598–1608CrossRefPubMedPubMedCentralGoogle Scholar
  20. Chmeliov J, Bricker WP, Lo C, Jouin E, Valkunas L, Ruban AV, Duffy CD (2015) An “all pigment” model of excitation quenching in LHCII. Phys Chem Chem Phys 17:15857–15867CrossRefPubMedGoogle Scholar
  21. Corpas FJ (2015) What is the role of hydrogen peroxide in plant peroxisomes? Plant Biol 17:1099–1103CrossRefPubMedGoogle Scholar
  22. Cueto-Ginzo AI, Serrano L, Bostock RM, Ferrio JP, Rodríguez R, Arcal L, Achon MÁ, Falcioni T, Luzuriaga WP, Medina V (2016) Salicylic acid mitigates physiological and proteomic changes induced by the SPCP1 strain of Potato virus X in tomato plants. Physiol Mol Plant Pathol 93:1–11CrossRefGoogle Scholar
  23. de Torres Zabala M, Littlejohn G, Jayaraman S, Studholme D, Bailey T, Lawson T, Tillich M, Licht D, Bölter B, Delfino L, Truman W, Mansfield J, Smirnoff N, Grant M (2015) Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nat Plant 1:15074CrossRefGoogle Scholar
  24. Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. BBA—Bioenergy 1020:1–24CrossRefGoogle Scholar
  25. Di Carli M, Villani ME, Bianco L, Lombardi R, Perrotta G, Benvenuto E, Donini M (2010) Proteomic analysis of the plant–virus interaction in Cucumber Mosaic Virus (CMV) resistant transgenic tomato. J Proteome Res 9:5684–5697CrossRefPubMedGoogle Scholar
  26. Di Carli M, Benvenuto E, Donini M (2012) Recent insights into plant–virus interactions through proteomic analysis. J Proteome Res 11:4765–4780CrossRefPubMedGoogle Scholar
  27. Diaz-Pendon JA, Truniger V, Nieto C, Garcia-Mas J, Bendahmane A, Aranda MA (2004) Advances in understanding recessive resistance to plant viruses. Mol Plant Pathol 5:223–233CrossRefPubMedGoogle Scholar
  28. Elrad D, Niyogi KK, Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14:1801–1816CrossRefPubMedPubMedCentralGoogle Scholar
  29. Elvira M, Galdeano MM, Gilardi P, García-Luque I, Serra MT (2008) Proteomic analysis of pathogenesis-related proteins (PRs) indeuced by compatible and incompatible interactions of pepper mild mottle virus (PMMoV) in Capsicum chinese L.3 plants. J Exp Bot 59:1253–1265CrossRefPubMedGoogle Scholar
  30. Foyer CH (2018) Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ Exp Bot 154:134–142CrossRefPubMedPubMedCentralGoogle Scholar
  31. Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364CrossRefGoogle Scholar
  32. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661CrossRefPubMedGoogle Scholar
  33. García-Murria MJ, Sudhani HPK, Marín-Navarro J, del Pino MMS, Moreno J (2018) Dissecting the individual contribution of conserved cysteines to the redox regulation of Rubisco. Photosynth Res 137:251–262CrossRefPubMedGoogle Scholar
  34. Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, Carrington JC (2010) Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during turnip mosaic virus infection. Plant Cell 22:481–496CrossRefPubMedPubMedCentralGoogle Scholar
  35. Garcia-Ruiz H, Garcia Ruiz MT, Peralta G, Manuel S, Gabriel M, Betzabeth C, El-Mounadi K (2016) Mecanismos, aplicaciones y perspectivas del silenciamiento génico de virus en plantas. Rev Mex Fitopatol 34:286–307Google Scholar
  36. Garcia-Ruiz H, Peralta GSM, Harte-Maxwell PA (2018) Tomato spotted wilt virus NSs protein supports infection and systemic movement of a potyviruses and is a symptom determinant. Viruses 10:1–21Google Scholar
  37. Hodgson RA, Beachy RN, Pakrasi HB (1989) Selective inhibition of photosystem II in spinach by tobacco mosaic virus: an effect of the viral coat protein. FEBS Lett 245:267–270CrossRefPubMedGoogle Scholar
  38. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684CrossRefPubMedGoogle Scholar
  39. Huang T-S, Wei T, Laliberté J-F, Wang A (2010) A host RNA helicase-like protein, AtRH8, interacts with the potyviral genome-linked protein, VPg, associates with the virus accumulation complex, and is essential for infection. Plant Physiol 152:255–266CrossRefPubMedPubMedCentralGoogle Scholar
  40. Huang Y, Ma HY, Huang W, Wang F, Xu ZS, Xiong AS (2016) Comparative proteomic analysis provides novel insight into the interaction between resistant vs susceptible tomato cultivars and TYLCV infection. BMC Plant Biol 16:162CrossRefPubMedPubMedCentralGoogle Scholar
  41. Huang W, Tikkanen M, Zhang SB (2018) Photoinhibition of photosystem I in Nephrolepis falciformis depends on reactive oxygen species generated in the chloroplast stroma. Photosynth Res 137:129–140CrossRefPubMedGoogle Scholar
  42. Hwang J, Lee S, Lee JH, Kang WH, Kang JH, Kang MY, Oh CS, Kang BC (2015) Plant translation elongation factor 1Bβ facilitates potato virus X (PVX) infection and interacts with PVX triple gene block protein 1. PLoS ONE 10:e0128014CrossRefPubMedPubMedCentralGoogle Scholar
  43. Jimbo H, Yutthanasirikul R, Nagano T, Hisabori T, Hihara Y, Nishiyama Y (2018) Oxidation of translation factor EF-Tu inhibits the repair of photosystem II. Plant Physiol 176:2691–2699CrossRefPubMedGoogle Scholar
  44. Johnson MP, Ruban AV (2010) Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J 61:283–289CrossRefPubMedGoogle Scholar
  45. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323CrossRefPubMedGoogle Scholar
  46. Kale R, Hebert AE, Frankel LK, Sallans L, Bricker TM, Pospíšil P (2017) Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of photosystem II. Proc Natl Acad Sci 114:2988–2993CrossRefPubMedGoogle Scholar
  47. Kangasjärvi S, Neukermans J, Li S, Aro E-M, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63:1619–1636CrossRefPubMedGoogle Scholar
  48. Karpiński S, Szechyńska-Hebda M, Wituszyńska W, Burdiak P (2013) Light acclimation, retrograde signalling, cell death and immune defences in plants. Plant Cell Environ 36:736–744CrossRefPubMedGoogle Scholar
  49. Kozuleva M, Goss T, Twachtmann M, Rudi K, Trapka J, Selinski J, Ivanov B, Garapati P, Steinhoff HJ, Hase T, Scheibe R, Klare JP, Hanke GT (2016) Ferredoxin:NADP(H) oxidoreductase abundance and location influences redox poise and stress tolerance. Plant Physiol 172:1480–1493CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kundu S, Chakraborty D, Pal A (2011) Proteomic analysis of salicylic acid induced resistance to Mungbean yellow mosaic india virus in Vigna mungo. J Proteom 74:337–349CrossRefGoogle Scholar
  51. Kundu S, Chakraborty D, Kundu A, Pal A (2013) Proteomics approach combined with biochemical attributes to elucidate compatible and incompatible plant–virus interactions between Vigna mungo and Mungbean yellow mosaic india virus. Proteome Sci 11:15CrossRefPubMedPubMedCentralGoogle Scholar
  52. Laliberté J-F, Sanfaçon H (2010) Cellular remodeling during plant virus infection. Annu Rev Phytopathol 48:69–91CrossRefPubMedGoogle Scholar
  53. Lin J-W, Ding M-P, Hsu Y-H, Tsai C-H (2006) Chloroplast phosphoglycerate kinase, a gluconeogenetic enzyme, is required for efficient accumulation of Bamboo mosaic virus. Nucl Acids Res 35:424–432CrossRefPubMedGoogle Scholar
  54. Liu J, Yang J, Bi H, Zhang P (2014) Why mosaic? Gene expression profiling of African Cassava Mosaic Virus-infected cassava reveals the effect of chlorophyll degradation on symptom development. J Integr Plant Biol 56:122–132CrossRefPubMedGoogle Scholar
  55. Lodha TD, Hembram P, Nitile Tep JB (2013) Proteomics: a successful approach to understand the molecular mechanism of plant-pathogen interaction. Am J Plant Sci 4:1212–1226CrossRefGoogle Scholar
  56. Lundin B, Thuswaldner S, Shutova T, Eshaghi S, Samuelsson G, Barber J, Andersson B, Spetea C (2007) Subsequent events to GTP binding by the plant PsbO protein: structural changes, GTP hydrolysis and dissociation from the photosystem II complex. Biochim Biophys Acta 1767:500–508CrossRefPubMedGoogle Scholar
  57. Mehta A, Brasileiro AC, Souza DS, Romano E, Campos MA, Grossi-de-Sá MF, Silva MS, Franco OL, Fragoso RR, Bevitori R, Rocha TL (2008) Plant–pathogen interactions: what is proteomics telling us? FEBS J 275:3731–3746CrossRefPubMedGoogle Scholar
  58. Mochizuki T, Ogata Y, Hirata Y, Ohki ST (2014) Quantitative transcriptional changes associated with chlorosis severity in mosaic leaves of tobacco plants infected with Cucumber mosaic virus. Mol Plant Pathol 15:242–254CrossRefPubMedGoogle Scholar
  59. Montasser M, Al-Ajmy A (2015) Histopathology for the influence of CMV infection on tomato cellular structures. FASEB J 29:887Google Scholar
  60. Nagy PD (2008) Yeast as a model host to explore plant virus–host interactions. Annu Rev Phytopathol 46:217–242CrossRefPubMedGoogle Scholar
  61. Nagy PD, Pogany J (2012) The dependence of viral RNA replication on co-opted host factors. Nat Rev Microbiol 10:137–149CrossRefGoogle Scholar
  62. Neilson EH, Goodger JQ, Woodrow IE, Møller BL (2013) Plant chemical defense: at what cost? Trends Plant Sci 18:250–258CrossRefPubMedGoogle Scholar
  63. Niehl A, Zhang ZJ, Kuiper M, Peck SC, Heinlein M (2013) Label-free quantitative proteomic analysis of systemic responses to local wounding and virus infection in Arabidopsis thaliana. J Proteome Res 12:2491–2503CrossRefPubMedGoogle Scholar
  64. Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382CrossRefPubMedGoogle Scholar
  65. Ouibrahim L, Mazier M, Estevan J, Pagny G, Decroocq V, Desbiez C, Moretti A, Gallois JL, Caranta C (2014) Cloning of the Arabidopsis rwm1 gene for resistance to Watermelon mosaic virus points to a new function for natural virus resistance genes. Plant J 79:705–716CrossRefPubMedGoogle Scholar
  66. Paiva AL, Oliveira JT, de Souza GA, Vasconcelos IM (2016) Label-free proteomic reveals that Cowpea Severe Mosaic Virus transiently suppresses the host leaf protein accumulation during the compatible interaction with cowpea (Vigna unguiculata [L.] Walp.). J Proteome Res 15:4208–4220CrossRefPubMedGoogle Scholar
  67. Pérez-Bueno ML, Rahoutei J, Sajnani C, García-Luque I, Barón M (2004) Proteomic analysis of the oxygen-evolving complex of photosystem II under biotec stress: studies on Nicotiana benthamiana infected with tobamoviruses. Proteomics 4:418–425CrossRefPubMedGoogle Scholar
  68. Pérez-Bueno ML, Ciscato M, García-Luque I, Valcke R, Barón M (2006) Imaging viral infection: studies on Nicotiana benthamiana plants infected with the pepper mild mottle tobamovirus. Photosynth Res 90:111–123CrossRefPubMedGoogle Scholar
  69. Peterhansel C, Krause K, Braun HP, Espie GS, Fernie AR, Hanson DT, Keech O, Maurino VG, Mielewczik M, Sage RF (2013) Engineering photorespiration: current state and future possibilities. Plant Biol 15:754–758CrossRefPubMedGoogle Scholar
  70. Pineda M, Sajnani C, Barón M (2010) Changes induced by the Pepper mild mottle tobamovirus on the chloroplast proteome of Nicotiana benthamiana. Photosynth Res 103:31–45CrossRefPubMedGoogle Scholar
  71. Prod’homme D, Le Panse S, Drugeon G, Jupin I (2001) Detection and subcellular localization of the turnip yellow mosaic virus 66 K replication protein in infected cells. Virology 281:88–101CrossRefPubMedGoogle Scholar
  72. Prod’homme D, Jakubiec A, Tournier V, Drugeon G, Jupin I (2003) Targeting of the turnip yellow mosaic virus 66 K replication protein to the chloroplast envelope is mediated by the 140 K protein. J Virol 77:9124–9135CrossRefPubMedPubMedCentralGoogle Scholar
  73. Qiu Y, Zhang Y, Wang C, Lei R, Wu Y, Li X, Zhu S (2018) Cucumber mosaic virus coat protein induces the development of chlorotic symptoms through interacting with the chloroplast ferredoxin I protein. Sci Rep 8:1205CrossRefPubMedPubMedCentralGoogle Scholar
  74. Quirino B, Candido E, Campos P, Franco O, Krüger R (2010) Proteomic approaches to study plant–pathogen interactions. Phytochemistry 71:351–362CrossRefPubMedGoogle Scholar
  75. Rahoutei J, García-Luque I, Barón M (2000) Inhibition of photosynthesis by viral infection: effect on PSII structure and function. Physiol Plant 110:286–292CrossRefGoogle Scholar
  76. Reinero A, Beachy RN (1989) Reduced photosystem II activity and accumulation of viral coat protein in chloroplasts of leaves infected with tobacco mosaic virus. Plant Physiol 89:111–116CrossRefPubMedPubMedCentralGoogle Scholar
  77. Roose JL, Frankel LK, Mummadisetti MP, Bricker TM (2016) The extrinsic proteins of photosystem II: update. Planta 243:889–908CrossRefPubMedGoogle Scholar
  78. Ruban AV (2017) Quantifying the efficiency of photoprotection. Philos Trans R Soc B Biol Sci 372:20160393CrossRefGoogle Scholar
  79. Ruban AV, Wentworth M, Yakushevska AE, Andersson J, Lee PJ, Keegstra W, Dekker JP, Boekema EJ, Jansson S, Horton P (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421:648–652CrossRefPubMedGoogle Scholar
  80. Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578CrossRefPubMedGoogle Scholar
  81. Ruban AV, Johnson MP, Duffy CDPP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181CrossRefPubMedGoogle Scholar
  82. Sato S, Nakamura Y, Kaneko T, Asamizu Tabata S (1999) Complete Structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 290:283–290CrossRefGoogle Scholar
  83. Serra-Soriano M, Navarro JA, Genoves A, Pallás V (2015) Comparative proteomic analysis of melon phloem exudates in response to viral infection. J Proteom 124:11–24CrossRefGoogle Scholar
  84. Shen J-R (2015) The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu Rev Plant Biol 66:23–48CrossRefPubMedGoogle Scholar
  85. Shimura H, Pantaleo V, Ishihara T, Myojo N, Inaba J-I, Sueda K, 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:e1002021CrossRefPubMedPubMedCentralGoogle Scholar
  86. Shitov AV, Pobeguts OV, Smolova TN, Allakhverdiev SI, Klimovet VV (2009) Manganese-dependent carboanhydrase activity of photosystem II proteins. Biochemistry 74:509–517PubMedGoogle Scholar
  87. Silveira JAG, Carvalho FEL (2016) Proteomics, photosynthesis and salt resistance in crops: an integrative view. J Proteom 143:24–35CrossRefGoogle Scholar
  88. Souza PF, Silva FD, Carvalho FE, Silveira JA, Vasconcelos IM, Oliveira JT (2017) Photosynthetic and biochemical mechanisms of an EMS-mutagenized cowpea associated with its resistance to Cowpea severe mosaic virus. Plant Cell Rep 36:219–234CrossRefPubMedGoogle Scholar
  89. Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53:449–475CrossRefPubMedGoogle Scholar
  90. Tajima Y, Iwakawa H-O, Hyodo K, Kaido M, Mise K, Okuno T (2017) Requirement for eukaryotic translation initiation factors in cap-independent translation differs between bipartite genomic RNAs of red clover necrotic mosaic virus. Virology 509:152–158CrossRefPubMedGoogle Scholar
  91. Takagi D, Takumi S, Hashiguchi M, Sejima T, Miyake C (2016) Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol 171:1626–1634CrossRefPubMedPubMedCentralGoogle Scholar
  92. Toby TK, Fornelli L, Kelleher NL (2016) Progress in top-down proteomics and the analysis of proteoforms. Annu Rev Anal Chem 9:499–519CrossRefGoogle Scholar
  93. Van Amerongen H, Croce R (2013) Light harvesting in photosystem II. Photosynth Res 116:251–263CrossRefPubMedPubMedCentralGoogle Scholar
  94. Varela ALN, Komatsu S, Wang X, Silva RGG, Souza PFN, Lobo AKM, Vasconcelos IM, Silveira JAG, Oliveira JTA (2017) Gel-free/label-free proteomic, photosynthetic, and biochemical analysis of cowpea (Vigna unguiculata [L.] Walp.) resistance against Cowpea severe mosaic virus (CPSMV). J Proteom 163:76–91CrossRefGoogle Scholar
  95. Varela ALN, Oliveira JTA, Komatsu S et al (2018) A resistant cowpea (Vigna unguiculata [L.] Walp.) genotype became susceptible to cowpea severe mosaic virus (CPSMV) after exposure to salt stress. J Proteom. CrossRefGoogle Scholar
  96. Ventelon-Debout M, Delalande F, Brizard JP, Diemer H, Van Dorsselaer A, Brugidou C (2004) Proteome analysis of cultivar-specific deregulations of Oryza sativa indica and O. sativa japonica cellular suspensions undergoing Rice yellow mottle virus infection. Proteomics 4:216–225CrossRefPubMedGoogle Scholar
  97. Voinnet O (2001) RNA silencing as a plant immune system against viruses. Trends Genet 17:449–459CrossRefPubMedGoogle Scholar
  98. Walker CJ, Weinstein JD (1991) In vitro assay of the chlorophyll biosynthetic enzyme Mg-chelatase: resolution of the activity into soluble and membrane-bound fractions. Proc Natl Acad Sci 88:5789–5793CrossRefPubMedGoogle Scholar
  99. Walker JC, Willows DR (1997) Mechanism and regulation of Mg-chelatase. Biochem J 327:321–333CrossRefPubMedPubMedCentralGoogle Scholar
  100. Walsh D, Mohr I (2011) Viral subversion of the host protein synthesis machinery. Nat Rev Microbiol 9:860CrossRefPubMedGoogle Scholar
  101. Wang A (2015) Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu Rev Phytopathol 53:45–66CrossRefPubMedGoogle Scholar
  102. Wang B, Ren Y, Lu C, Wang X (2015) iTRAQ-based quantitative proteomics analysis of rice leaves infected by Rice stripe virus reveals several proteins involved in symptom formation. Virol J 12:99CrossRefPubMedPubMedCentralGoogle Scholar
  103. Wang J, X-r Wang, Zhou Q, J-m Yang, H-x Guo, L-j Yang, W-q Liu (2016) iTRAQ protein profile analysis provides integrated insight into mechanisms of tolerance to TMV in tobacco (Nicotiana tabacum). J Proteom 132:21–30CrossRefGoogle Scholar
  104. Wei T, Zhang C, Hou X, Sanfaçon H, Wang A (2013) The SNARE protein Syp71 is essential for turnip mosaic virus infection by mediating fusion of virus-induced vesicles with chloroplasts. PLoS Pathog 9:e1003378CrossRefPubMedPubMedCentralGoogle Scholar
  105. Whitfield AE, Falk BW, Rotenberg D (2015) Insect vector-mediated transmission of plant viruses. Virology 480:278–289CrossRefGoogle Scholar
  106. Wu L, Han Z, Wang S, Wang X, Sun A, Zu X, Chen Y (2013) Comparative proteomic analysis of the plant–virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. J Proteomics 89:124–140CrossRefPubMedGoogle Scholar
  107. Xu Q, Ni H, Chen Q, Sun F, Zhou T, Lan Y, Zhou Y (2013) Comparative proteomic analysis reveals the cross-talk between the responses induced by H2O2 and by long-term Rice black-streaked dwarf virus infection in Rice. PLoS ONE 8:e81640CrossRefPubMedPubMedCentralGoogle Scholar
  108. Yang A, Yu L, Chen Z, Zhang S, Shi J, Zhao X, Yang Y, Hu D, Song B (2017) Label-free quantitative proteomic analysis of chitosan oligosaccharide-treated rice infected with southern rice black-streaked dwarf virus. Viruses 115:1–16Google Scholar
  109. Yi X, Hargett SR, Frankel LK, Bricker TM (2009) The PsbP protein, but not the PsbQ protein, is required for normal thylakoid architecture in Arabidopsis thaliana. FEBS Lett 583:2142–2147CrossRefPubMedGoogle Scholar
  110. Zhao J, Zhang X, Hong Y, Liu Y (2016) Chloroplast in plant–virus interaction. Front Microbiol 7:1565PubMedPubMedCentralGoogle Scholar
  111. Zhong X, Wang ZQ, Xiao R, Wang Y, Xie Y, Zhou X (2017) iTRAQ analysis of the tobacco leaf proteome reveals that RNA-directed DNA methylation (RdDM) has important roles in defense against geminivirus-betasatellite infection. J Proteom 152:88–101CrossRefGoogle Scholar

Copyright information

© Brazilian Society of Plant Physiology 2019

Authors and Affiliations

  • Pedro F. N. Souza
    • 1
    • 2
  • Hernan Garcia-Ruiz
    • 1
  • Fabricio E. L. Carvalho
    • 2
    Email author
  1. 1.Department of Plant Pathology, Nebraska Center for VirologyUniversity of Nebraska-LincolnLincolnUSA
  2. 2.Department of Biochemistry and Molecular BiologyFederal University of CearáFortalezaBrazil

Personalised recommendations