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The interplay of plant hormonal pathways and geminiviral proteins: partners in disease development

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Abstract

Viruses belonging to the family Geminiviridae infect plants and are responsible for a number of diseases of crops in the tropical and sub-tropical regions of the World. The innate immune response of the plant assists in its defense against such viral pathogens by the recognition of pathogen/microbe-associated molecular patterns through pattern-recognition receptors. Phytohormone signalling pathways play a vital role in plant defense responses against these devastating viruses. Geminiviruses, however, have developed counter-defense strategies that prevail over the above defense pathways. The proteins encoded by geminiviruses act as suppressors of plant immunity by interacting with the signalling components of several hormones. In this review we focus on the molecular interplay of phytohormone pathways and geminiviral infection and try to find interesting parallels with similar mechanisms known in other plant-infecting viruses and strengthen the argument that this interplay is necessary for disease development.

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References

  1. Boutrot F, Zipfel C (2017) Function, discovery, and exploitation of plant pattern recognition receptors for broad spectrum disease resistance. Annu Rev Phytopathol 55:257–286

    Article  CAS  PubMed  Google Scholar 

  2. Ranf S (2017) Sensing of molecular patterns through cell surface immune receptors. Curr Opin Plant Biol 38:68–77. https://doi.org/10.1016/j.pbi.2017.04.011

    Article  CAS  PubMed  Google Scholar 

  3. Saijo Y, E. P. IIan Loo, and S. Yasuda, (2018) Pattern recognition receptors and signaling in plant–microbe interactions. Plant J 93(4):592–613. https://doi.org/10.1111/tpj.13808

    Article  CAS  PubMed  Google Scholar 

  4. Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8(4):521–539. https://doi.org/10.1016/j.molp.2014.12.022

    Article  CAS  PubMed  Google Scholar 

  5. Thulasi Devendrakumar K, Li X, Zhang Y (2018) MAP kinase signalling: interplays between plant PAMP- and effector-triggered immunity. Cell Mol Life Sci 75(16):2981–2989. https://doi.org/10.1007/s00018-018-2839-3

    Article  CAS  PubMed  Google Scholar 

  6. Nicaise V, Candresse T (2017) Plum pox virus capsid protein suppresses plant pathogen-associated molecular pattern (PAMP)-triggered immunity. Mol Plant Pathol 18(6):878–886. https://doi.org/10.1111/mpp.12447

    Article  CAS  PubMed  Google Scholar 

  7. Kong J et al (2018) The cucumber mosaic virus movement protein suppresses PAMP-triggered immune responses in Arabidopsis and tobacco. Biochem Biophys Res Commun 498(3):395–401. https://doi.org/10.1016/j.bbrc.2018.01.072

    Article  CAS  PubMed  Google Scholar 

  8. Niehl A, Wyrsch I, Boller T, Heinlein M (2016) Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol 211(3):1008–1019. https://doi.org/10.1111/nph.13944

    Article  CAS  PubMed  Google Scholar 

  9. Amari K, Niehl A (2020) Nucleic acid-mediated PAMP-triggered immunity in plants. Curr Opin Virol 42:32–39. https://doi.org/10.1016/j.coviro.2020.04.003

    Article  CAS  PubMed  Google Scholar 

  10. Jones JDJ, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329

    Article  CAS  PubMed  Google Scholar 

  11. Caplan J, Padmanabhan M, Dinesh-Kumar SP (2008) Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3(3):126–135. https://doi.org/10.1016/j.chom.2008.02.010

    Article  CAS  PubMed  Google Scholar 

  12. Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol. https://doi.org/10.1146/annurev-arplant-050213-040012

    Article  PubMed  Google Scholar 

  13. Bürger M, Chory J (2019) Stressed out about hormones: how plants orchestrate immunity. Cell Host Microbe 26(2):163–172. https://doi.org/10.1016/j.chom.2019.07.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459(7250):1071–1078. https://doi.org/10.1038/nature08122

    Article  CAS  PubMed  Google Scholar 

  15. Pieterse CMJ, Van Der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28(April):489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055

    Article  CAS  PubMed  Google Scholar 

  16. Alazem M, Lin NS (2015) Roles of plant hormones in the regulation of host-virus interactions. Mol Plant Pathol 16(5):529–540. https://doi.org/10.1111/mpp.12204

    Article  CAS  PubMed  Google Scholar 

  17. Ma KW, Ma W (2016) Phytohormone pathways as targets of pathogens to facilitate infection. Plant Mol Biol 91(6):713–725. https://doi.org/10.1007/s11103-016-0452-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Islam W, Naveed H, Zaynab M, Huang Z, Chen HYH (2019) Plant defense against virus diseases; growth hormones in highlights. Plant Signal Behav 14(6):1–10. https://doi.org/10.1080/15592324.2019.1596719

    Article  CAS  Google Scholar 

  19. Rojas MR et al (2018) World Management of Geminiviruses. Annu Rev Phytopathol 56:637–677. https://doi.org/10.1146/annurev-phyto-080615-100327

    Article  CAS  PubMed  Google Scholar 

  20. Varsani A et al (2014) Establishment of three new genera in the family Geminiviridae: Becurtovirus, Eragrovirus and Turncurtovirus. Arch Virol 159(8):2193–2203. https://doi.org/10.1007/s00705-014-2050-2

    Article  CAS  PubMed  Google Scholar 

  21. Zerbini FM et al (2017) ICTV virus taxonomy profile: Geminiviridae. J Gen Virol 98(2):131–133. https://doi.org/10.1099/jgv.0.000738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gnanasekaran P, KishoreKumar R, Bhattacharyya D, Vinoth Kumar R, Chakraborty S (2019) Multifaceted role of geminivirus associated betasatellite in pathogenesis. Mol Plant Pathol 20(7):1019–1033. https://doi.org/10.1111/mpp.12800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Van Wezel R, Dong X, Blake P, Stanley J, Hong Y (2002) Differential roles of geminivirus Rep and AC4 (C4) in the induction of necrosis in Nicotiana benthamiana. Mol Plant Pathol 3(6):461–471. https://doi.org/10.1046/j.1364-3703.2002.00141.x

    Article  PubMed  Google Scholar 

  24. Hussain M, Mansoor S, Iram S, Zafar Y, Briddon RW (2007) The hypersensitive response to tomato leaf curl New Delhi virus nuclear shuttle protein is inhibited by transcriptional activator protein. Mol Plant-Microbe Interact 20(12):1581–1588. https://doi.org/10.1094/MPMI-20-12-1581

    Article  CAS  PubMed  Google Scholar 

  25. Sharma P, Ikegami M (2010) Tomato leaf curl Java virus V2 protein is a determinant of virulence, hypersensitive response and suppression of posttranscriptional gene silencing. Virology 396(1):85–93. https://doi.org/10.1016/j.virol.2009.10.012

    Article  CAS  PubMed  Google Scholar 

  26. Saeed F et al (2018) Infectivity of okra enation leaf curl virus and the role of its V2 protein in pathogenicity. Virus Res 255(January):90–94. https://doi.org/10.1016/j.virusres.2018.07.007

    Article  CAS  PubMed  Google Scholar 

  27. Shine MB, Xiao X, Kachroo P, Kachroo A (2019) Signaling mechanisms underlying systemic acquired resistance to microbial pathogens. Plant Sci 279:81–86. https://doi.org/10.1016/j.plantsci.2018.01.001

    Article  CAS  PubMed  Google Scholar 

  28. Ghosh D, Chakraborty S (2021) Molecular interplay between phytohormones and geminiviruses: a saga of a never-ending arms race. J Exp Bot 72(8):2903–2917. https://doi.org/10.1093/jxb/erab061

    Article  CAS  PubMed  Google Scholar 

  29. Gupta N, Reddy K, Bhattacharyya D, Chakraborty S (2021) Plant responses to geminivirus infection: guardians of the plant immunity. Virol J 18(1):1–25. https://doi.org/10.1186/s12985-021-01612-1

    Article  CAS  Google Scholar 

  30. Qi G et al (2018) Pandemonium Breaks Out: Disruption of Salicylic Acid-Mediated Defense by Plant Pathogens. Mol Plant 11(12):1427–1439. https://doi.org/10.1016/j.molp.2018.10.002

    Article  CAS  PubMed  Google Scholar 

  31. Janda T, Szalai G, Pál M (2020) Salicylic acid signalling in plants. Int J Mol Sci. https://doi.org/10.3390/ijms21072655

    Article  PubMed  PubMed Central  Google Scholar 

  32. Ding P, Ding Y (2020) Stories of salicylic acid: a plant defense hormone. Trends Plant Sci 25(6):549–565. https://doi.org/10.1016/j.tplants.2020.01.004

    Article  CAS  PubMed  Google Scholar 

  33. Lefevere H, Bauters L, Gheysen G (2020) Salicylic Acid Biosynthesis in Plants. Front Plant Sci 11(April):1–7. https://doi.org/10.3389/fpls.2020.00338

    Article  Google Scholar 

  34. Tada Y et al (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321(5891):952–956. https://doi.org/10.1126/science.1156970

    Article  CAS  PubMed  Google Scholar 

  35. Zhou JM et al (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant-Microbe Interact 13(2):191–202. https://doi.org/10.1094/MPMI.2000.13.2.191

    Article  CAS  PubMed  Google Scholar 

  36. Li N, Han X, Feng D, Yuan D, Huang LJ (2019) Signaling crosstalk between salicylic acid and ethylene/Jasmonate in plant defense: do we understand what they are whispering? Int J Mol Sci. https://doi.org/10.3390/ijms20030671

    Article  PubMed  PubMed Central  Google Scholar 

  37. Pokotylo I, Kravets V, Ruelland E (2019) Salicylic acid binding proteins (SABPs): the hidden forefront of salicylic acid signalling. Int J Mol Sci 20(18):1–20. https://doi.org/10.3390/ijms20184377

    Article  CAS  Google Scholar 

  38. Alamillo JM, Saénz P, García JA (2006) Salicylic acid-mediated and RNA-silencing defense mechanisms cooperate in the restriction of systemic spread of plum pox virus in tobacco. Plant J 48(2):217–227. https://doi.org/10.1111/j.1365-313X.2006.02861.x

    Article  CAS  PubMed  Google Scholar 

  39. Agudelo-Romero P et al (2008) Changes in the gene expression profile of Arabidopsis thaliana after infection with tobacco etch virus. Virol J 5:1–11. https://doi.org/10.1186/1743-422X-5-92

    Article  CAS  Google Scholar 

  40. Chen H et al (2010) Up-regulation of LSB1/GDU3 affects geminivirus infection by activating the salicylic acid pathway. Plant J 62(1):12–23. https://doi.org/10.1111/j.1365-313X.2009.04120.x

    Article  CAS  PubMed  Google Scholar 

  41. Rodriguez MC, Conti G, Zavallo D, Manacorda CA, Asurmendi S (2014) TMV-Cg Coat Protein stabilizes DELLA proteins and in turn negatively modulates salicylic acid-mediated defense pathway during Arabidopsis thaliana viral infection. BMC Plant Biol 14(1):1–17. https://doi.org/10.1186/s12870-014-0210-x

    Article  CAS  Google Scholar 

  42. Tian M et al (2015) Salicylic acid inhibits the replication of tomato bushy stunt virus by directly targeting a host component in the replication complex. Mol Plant-Microbe Interact 28(4):379–386. https://doi.org/10.1094/MPMI-09-14-0259-R

    Article  CAS  PubMed  Google Scholar 

  43. K. Li et al., 2018 “Transcriptome analysis of Nicotiana benthamiana infected by Tobacco curly shoot virus,” Viro. J Doi: https://doi.org/10.1186/s12985-018-1044-1

  44. Wang D, Zhang X, Yao X, Zhang P, Fang R, Ye J (2020) A 7-amino-acid motif of REp protein essential for virulence is critical for triggering host defense against Sri Lankan cassava mosaic virus. Mol Plant-Microbe Interact 33(1):78–86. https://doi.org/10.1094/MPMI-06-19-0163-FI

    Article  CAS  PubMed  Google Scholar 

  45. Ascencio-Ibáñez JT et al (2008) Global analysis of arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 148(1):436–454. https://doi.org/10.1104/pp.108.121038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Miozzi L, Napoli C, Sardo L, Accotto GP (2014) Transcriptomics of the interaction between the monopartite phloem-limited geminivirus tomato yellow leaf curl sardinia virus and solanum lycopersicum highlights a role for plant hormones, autophagy and plant immune system fine tuning during infection. PLoS ONE. https://doi.org/10.1371/journal.pone.0089951

    Article  PubMed  PubMed Central  Google Scholar 

  47. Yang LP et al (2013) C2-mediated decrease in DNA methylation, accumulation of siRNAs, and increase in expression for genes involved in defense pathways in plants infected with beet severe curly top virus. Plant J 73(6):910–917. https://doi.org/10.1111/tpj.12081

    Article  CAS  PubMed  Google Scholar 

  48. Tu YC et al (2017) The C2 protein of tomato leaf curl Taiwan virus is a pathogenicity determinant that interferes with expression of host genes encoding chromomethylases. Physiol Plant 161(4):515–531. https://doi.org/10.1111/ppl.12615

    Article  CAS  PubMed  Google Scholar 

  49. Guerrero J, Regedanz E, Lu L, Ruan J, Bisaro DM, Sunter G (2020) Manipulation of the plant host by the Geminivirus AC2/C2 protein, a central player in the infection cycle. Front Plant Sci 11(May):1–18. https://doi.org/10.3389/fpls.2020.00591

    Article  Google Scholar 

  50. Matić S, Pegoraro M, Noris E (2016) The C2 protein of tomato yellow leaf curl Sardinia virus acts as a pathogenicity determinant and a 16-amino acid domain is responsible for inducing a hypersensitive response in plants. Virus Res 215:12–19. https://doi.org/10.1016/j.virusres.2016.01.014

    Article  CAS  PubMed  Google Scholar 

  51. Shi X et al (2013) Plant virus differentially alters the plant’s defense response to its closely related vectors. PLoS ONE 8(12):1–8. https://doi.org/10.1371/journal.pone.0083520

    Article  CAS  Google Scholar 

  52. C. Hettenhausen, M. C. Schuman, and J. Wu, “Europe PMC Funders Group Europe PMC Funders Author Manuscripts MAPK signaling – a key element in plant defense response to insects,” vol. 22, no. 2, pp. 157–164, 2017, doi: https://doi.org/10.1111/1744-7917.12128.MAPK

  53. Yu G et al (2020) A bacterial effector protein prevents mapk-mediated phosphorylation of sgt1 to suppress plant immunity. PLoS Pathog 16(9):1–30. https://doi.org/10.1371/journal.ppat.1008933

    Article  CAS  Google Scholar 

  54. Li Y et al (2017) SlMAPK3 enhances tolerance to tomato yellow leaf curl virus (TYLCV) by regulating salicylic acid and jasmonic acid signaling in tomato (Solanum lycopersicum). PLoS ONE 12(2):1–21. https://doi.org/10.1371/journal.pone.0172466

    Article  CAS  Google Scholar 

  55. Zhang L, Zhang F, Melotto M, Yao J, He SY (2017) Jasmonate signaling and manipulation by pathogens and insects. J Exp Bot 68(6):1371–1385. https://doi.org/10.1093/jxb/erw478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Wasternack C, Hause B (2013) Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111(6):1021–1058. https://doi.org/10.1093/aob/mct067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Fonseca S et al (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5(5):344–350. https://doi.org/10.1038/nchembio.161

    Article  CAS  PubMed  Google Scholar 

  58. J. Ruan et al., 2019 “Jasmonic acid signaling pathway in plants,” Int J Mo. Sci, doi: https://doi.org/10.3390/ijms20102479

  59. M. S. Ali and K. H. Baek, 2020 “Jasmonic acid signaling pathway in response to abiotic stresses in plants,” Int. J Mol Sci doi: https://doi.org/10.3390/ijms21020621

  60. Thines B et al (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448(7154):661–665. https://doi.org/10.1038/nature05960

    Article  CAS  PubMed  Google Scholar 

  61. Katsir L, Schilmiller AL, Staswick PE, Sheng YH, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 105(19):7100–7105. https://doi.org/10.1073/pnas.0802332105

    Article  PubMed  PubMed Central  Google Scholar 

  62. L. B. Sheard et al., 2011 “HHS Public Access,” vol. 468, no. 7322, pp. 400–405, , doi: https://doi.org/10.1038/nature09430.Jasmonate.

  63. Kazan K, Manners JM (2013) MYC2: the master in action. Mol Plant 6(3):686–703. https://doi.org/10.1093/mp/sss128

    Article  CAS  PubMed  Google Scholar 

  64. Xie Z, Nolan TM, Jiang H, Yin Y (2019) AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Front Plant Sci 10(February):1–17. https://doi.org/10.3389/fpls.2019.00228

    Article  Google Scholar 

  65. Wu X, Ye J (2020) Manipulation of jasmonate signaling by plant viruses and their insect vectors. Viruses 12(2):1–16. https://doi.org/10.3390/v12020148

    Article  CAS  Google Scholar 

  66. Góngora-Castillo E, Ibarra-Laclette E, Trejo-Saavedra DL, Rivera-Bustamante RF (2012) Transcriptome analysis of symptomatic and recovered leaves of geminivirus-infected pepper (Capsicum annuum). Virol J 9:1–16. https://doi.org/10.1186/1743-422X-9-295

    Article  CAS  Google Scholar 

  67. Csorba T, Kontra L, Burgyán J (2015) Viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence. Virology 479–480:85–103. https://doi.org/10.1016/j.virol.2015.02.028

    Article  CAS  PubMed  Google Scholar 

  68. Lozano-Durán R et al (2011) Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23(3):1014–1032. https://doi.org/10.1105/tpc.110.080267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Li T, Huang Y, Xu ZS, Wang F, Xiong AS (2019) Salicylic acid-induced differential resistance to the tomato yellow leaf curl virus among resistant and susceptible tomato cultivars. BMC Plant Biol 19(1):1–14. https://doi.org/10.1186/s12870-019-1784-0

    Article  Google Scholar 

  70. Jia Q et al (2016) CLCuMuB βC1 Subverts Ubiquitination by Interacting with NbSKP1s to Enhance Geminivirus Infection in Nicotiana benthamiana. PLoS Pathog 12(6):1–30. https://doi.org/10.1371/journal.ppat.1005668

    Article  CAS  Google Scholar 

  71. Zou C et al (2020) Begomovirus-associated betasatellite virulence factor βC1 attenuates tobacco defense to whiteflies via interacting with plant SKP1. Front Plant Sci 11(August):1–11. https://doi.org/10.3389/fpls.2020.574557

    Article  Google Scholar 

  72. Li Y et al (2019) Interaction between Brassica yellows virus silencing suppressor P0 and plant SKP1 facilitates stability of P0 in vivo against degradation by proteasome and autophagy pathways. New Phytol 222(3):1458–1473. https://doi.org/10.1111/nph.15702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Chen S et al (2019) Cucurbit chlorotic yellows virus p22 protein interacts with cucumber SKP1LB1 and its F-box-like motif is crucial for silencing suppressor activity. Viruses. https://doi.org/10.3390/v11090818

    Article  PubMed  PubMed Central  Google Scholar 

  74. He L et al (2020) Rice black-streaked dwarf virus-encoded P5–1 regulates the ubiquitination activity of SCF E3 ligases and inhibits jasmonate signaling to benefit its infection in rice. New Phytol 225(2):896–912. https://doi.org/10.1111/nph.16066

    Article  CAS  PubMed  Google Scholar 

  75. Wu D et al (2017) Viral effector protein manipulates host hormone signaling to attract insect vectors. Cell Res 27(3):402–415. https://doi.org/10.1038/cr.2017.2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17(6):349–359. https://doi.org/10.1016/j.tplants.2012.03.001

    Article  CAS  PubMed  Google Scholar 

  77. Wasternack C, Strnad M (2019) Jasmonates are signals in the biosynthesis of secondary metabolites — Pathways, transcription factors and applied aspects — A brief review. N Biotechnol 48(September):1–11. https://doi.org/10.1016/j.nbt.2017.09.007

    Article  CAS  PubMed  Google Scholar 

  78. Luan JB et al (2013) Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecol Lett 16(3):390–398. https://doi.org/10.1111/ele.12055

    Article  PubMed  Google Scholar 

  79. Li R et al (2014) Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance. Plant Cell 26(12):4991–5008. https://doi.org/10.1105/tpc.114.133181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Rosas-Díaz T, Macho AP, Beuzón CR, Lozano-Durán R, Bejarano ER (2016) The C2 protein from the geminivirus tomato yellow leaf curl sardinia virus decreases sensitivity to jasmonates and suppresses jasmonate-mediated defences. Plants 5(1):777–788. https://doi.org/10.3390/plants5010008

    Article  CAS  Google Scholar 

  81. Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, Chua NH (2008) βCl, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22(18):2564–2577. https://doi.org/10.1101/gad.1682208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Sun YC, Pan LL, Ying FZ, Li P, Wang XW, Liu SS (2017) Jasmonic acid-related resistance in tomato mediates interactions between whitefly and whitefly-transmitted virus. Sci Rep 7(1):1–7. https://doi.org/10.1038/s41598-017-00692-w

    Article  CAS  Google Scholar 

  83. Du J et al (2020) NSs, the silencing suppressor of tomato spotted wilt orthotospovirus, interferes with JA-regulated host terpenoids expression to attract Frankliniella occidentalis. Front Microbiol 11(December):1–12. https://doi.org/10.3389/fmicb.2020.590451

    Article  Google Scholar 

  84. Dubois M, Van den Broeck L, Inzé D (2018) The pivotal role of ethylene in plant growth. Trends Plant Sci 23(4):311–323. https://doi.org/10.1016/j.tplants.2018.01.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20(4):219–229. https://doi.org/10.1016/j.tplants.2015.02.001

    Article  CAS  PubMed  Google Scholar 

  86. Binder BM (2020) Ethylene signaling in plants. J Biol Chem 295(22):7710–7725. https://doi.org/10.1074/jbc.REV120.010854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Ju C, Chang C (2015) Mechanistic insights in ethylene perception and signal transduction. Plant Physiol 169(1):85–95. https://doi.org/10.1104/pp.15.00845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Bak A, Patton MKF, Perilla-Henao LM, Aegerter BJ, Casteel CL (2019) Ethylene signaling mediates potyvirus spread by aphid vectors. Oecologia 190(1):139–148. https://doi.org/10.1007/s00442-019-04405-0

    Article  PubMed  Google Scholar 

  89. Broekgaarden C, Caarls L, Vos IA, Pieterse CMJ, Van Wees SCM (2015) Ethylene: traffic controller on hormonal crossroads to defense. Plant Physiol 169(4):2371–2379. https://doi.org/10.1104/pp.15.01020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Soitamo AJ, Jada B, Lehto K (2012) Expression of geminiviral AC2 RNA silencing suppressor changes sugar and jasmonate responsive gene expression in transgenic tobacco plants. BMC Plant Biol 12(1):1. https://doi.org/10.1186/1471-2229-12-204

    Article  CAS  Google Scholar 

  91. Chen T et al (2013) Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PLoS ONE 8(11):4–6. https://doi.org/10.1371/journal.pone.0080816

    Article  CAS  Google Scholar 

  92. Wu M, Ding X, Fu X, Lozano-Duran R (2019) Transcriptional reprogramming caused by the geminivirus tomato yellow leaf curl virus in local or systemic infections in Nicotiana benthamiana. BMC Genomics 20(1):1–17. https://doi.org/10.1186/s12864-019-5842-7

    Article  CAS  Google Scholar 

  93. Song S, Qi T, Wasternack C, Xie D (2014) Jasmonate signaling and crosstalk with gibberellin and ethylene. Curr Opin Plant Biol 21:112–119. https://doi.org/10.1016/j.pbi.2014.07.005

    Article  CAS  PubMed  Google Scholar 

  94. Yang DL et al (2008) Altered disease development in the eui mutants and Eui overexpressors indicates that gibberellins negatively regulate rice basal disease resistance. Mol Plant 1(3):528–537. https://doi.org/10.1093/mp/ssn021

    Article  CAS  PubMed  Google Scholar 

  95. Qi T et al (2014) Arabidopsis DELLA and JAZ proteins bind the WD-Repeat/ bHLH/MYB complex to modulate gibberellin and jasmonate signaling synergy. Plant Cell 26(3):1118–1133. https://doi.org/10.1105/tpc.113.121731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Davière JM, Achard P (2013) Gibberellin signaling in plants. Dev 140(6):1147–1151. https://doi.org/10.1242/dev.087650

    Article  CAS  Google Scholar 

  97. Bao S, Hua C, Shen L, Yu H (2020) New insights into gibberellin signaling in regulating flowering in Arabidopsis. J Integr Plant Biol 62(1):118–131. https://doi.org/10.1111/jipb.12892

    Article  CAS  PubMed  Google Scholar 

  98. Hofmann NR (2016) A structure for plant-specific transcription factors: the gras domain revealed. Plant Cell 28(5):993–994. https://doi.org/10.1105/tpc.16.00309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Ito T, Okada K, Fukazawa J, Takahashi Y (2018) DELLA-dependent and -independent gibberellin signaling. Plant Signal Behav 13(3):1–3. https://doi.org/10.1080/15592324.2018.1445933

    Article  CAS  Google Scholar 

  100. Navarro L et al (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18(9):650–655. https://doi.org/10.1016/j.cub.2008.03.060

    Article  CAS  PubMed  Google Scholar 

  101. Achard P, Genschik P (2009) Releasing the brakes of plant growth: How GAs shutdown della proteins. J Exp Bot 60(4):1085–1092. https://doi.org/10.1093/jxb/ern301

    Article  CAS  PubMed  Google Scholar 

  102. Hauvermale AL, Ariizumi T, Steber CM (2012) Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol 160(1):83–92. https://doi.org/10.1104/pp.112.200956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. de Vleesschauwer D et al (2012) Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol 158(4):1833–1846. https://doi.org/10.1104/pp.112.193672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69(4):473–488. https://doi.org/10.1007/s11103-008-9435-0

    Article  CAS  PubMed  Google Scholar 

  105. Zhu S et al (2005) The rice dwarf virus P2 protein interacts with ent-kaurene oxidases in vivo, leading to reduced biosynthesis of gibberellins and rice dwarf symptoms. Plant Physiol 139(4):1935–1945. https://doi.org/10.1104/pp.105.072306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Lozano-Durán R, Rosas-Díaz T, Luna AP, Bejarano ER (2011) Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS ONE. https://doi.org/10.1371/journal.pone.0022383

    Article  PubMed  PubMed Central  Google Scholar 

  107. Mills-Lujan K, Deom CM (2010) Geminivirus C4 protein alters Arabidopsis development. Protoplasma 239(1–4):95–110. https://doi.org/10.1007/s00709-009-0086-z

    Article  CAS  PubMed  Google Scholar 

  108. Argueso CT et al (2012) Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002448

    Article  PubMed  PubMed Central  Google Scholar 

  109. E. Zürcher and B. Müller, 2016 Cytokinin Synthesis, Signaling, and Function-Advances and New Insights, Elsevier Inc

  110. Kieber JJ, Schaller GE (2018) Cytokinin signaling in plant development. Development 145(4):1–7. https://doi.org/10.1242/dev.149344

    Article  CAS  Google Scholar 

  111. Ashihara H, Stasolla C, Fujimura T, Crozier A (2018) Purine salvage in plants. Phytochemistry 147:89–124. https://doi.org/10.1016/j.phytochem.2017.12.008

    Article  CAS  PubMed  Google Scholar 

  112. Wang H, Buckley KJ, Yang X, Buchmann RC, Bisaro DM (2005) Adenosine kinase inhibition and suppression of RNA silencing by Geminivirus AL2 and L2 Proteins. J Virol 79(12):7410–7418. https://doi.org/10.1128/jvi.79.12.7410-7418.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Buchmann RC, Asad S, Wolf JN, Mohannath G, Bisaro DM (2009) Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 83(10):5005–5013. https://doi.org/10.1128/jvi.01771-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Baliji S, Lacatus G, Sunter G (2010) The Interaction between geminivirus pathogenicity proteins and adenosine kinase leads to increased expression of primary cytokinin-responsive genes. Virology 402(2):238–247. https://doi.org/10.1016/j.virol.2010.03.023

    Article  CAS  PubMed  Google Scholar 

  115. Seo JK et al (2018) Molecular dissection of distinct symptoms induced by tomato chlorosis virus and tomato yellow leaf curl virus based on comparative transcriptome analysis. Virology. https://doi.org/10.1016/j.virol.2018.01.001

    Article  PubMed  Google Scholar 

  116. Kim EJ, Russinova E (2020) Brassinosteroid signalling. Curr Biol 30(7):R294–R298. https://doi.org/10.1016/j.cub.2020.02.011

    Article  CAS  PubMed  Google Scholar 

  117. Li Z, He Y (2020) Roles of brassinosteroids in plant reproduction. Int J Mol Sci 21(3):1–16. https://doi.org/10.3390/ijms21030872

    Article  CAS  Google Scholar 

  118. Youn JH, Kim TW (2015) Functional insights of plant GSK3-like kinases: multi-taskers in diverse cellular signal transduction pathways. Mol Plant 8(4):552–565. https://doi.org/10.1016/j.molp.2014.12.006

    Article  CAS  PubMed  Google Scholar 

  119. Sun Y et al (2010) Integration of Brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19(5):765–777. https://doi.org/10.1016/j.devcel.2010.10.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Planas-Riverola A, Gupta A, Betegoń-Putze I, Bosch N, Ibanḛs M, Cano-Delgado AI (2019) Brassinosteroid signaling in plant development and adaptation to stress. Dev 146(5):1–11. https://doi.org/10.1242/dev.151894

    Article  CAS  Google Scholar 

  121. Ortiz-Morea FA, He P, Shan L, Russinova E (2020) It takes two to tango - Molecular links between plant immunity and brassinosteroid signalling. J Cell Sci 133(22):1–11. https://doi.org/10.1242/jcs.246728

    Article  CAS  Google Scholar 

  122. Zhang DW, Deng XG, Fu FQ, Lin HH (2015) Induction of plant virus defense response by brassinosteroids and brassinosteroid signaling in Arabidopsis thaliana. Planta 241(4):875–885. https://doi.org/10.1007/s00425-014-2218-8

    Article  CAS  PubMed  Google Scholar 

  123. C. Julie KØrner, et al (2013) The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. Mol Plant-Microbe Interact. https://doi.org/10.1094/MPMI-06-13-0179-R

    Article  Google Scholar 

  124. Park J et al (2011) The arabidopsis thaliana homeobox gene ATHB12 is involved in symptom development caused by geminivirus infection. PLoS ONE. https://doi.org/10.1371/journal.pone.0020054

    Article  PubMed  PubMed Central  Google Scholar 

  125. Deom CM, Alabady MS, Yang L (2021) Early transcriptome changes induced by the Geminivirus C4 oncoprotein: setting the stage for oncogenesis. BMC Genomics 22(1):1–19. https://doi.org/10.1186/s12864-021-07455-y

    Article  CAS  Google Scholar 

  126. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S (2013) Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 11(11):777–788. https://doi.org/10.1038/nrmicro3117

    Article  CAS  PubMed  Google Scholar 

  127. Mills-Lujan K, Andrews DL, Chou CW, Deom CM (2015) The roles of phosphorylation and SHAGGY-like protein kinases in geminivirus C4 protein induced hyperplasia. PLoS ONE 10(3):1–26. https://doi.org/10.1371/journal.pone.0122356

    Article  CAS  Google Scholar 

  128. Piroux N, Saunders K, Page A, Stanley J (2007) Geminivirus pathogenicity protein C4 interacts with Arabidopsis thaliana shaggy-related protein kinase AtSKη, a component of the brassinosteroid signalling pathway. Virology 362(2):428–440. https://doi.org/10.1016/j.virol.2006.12.034

    Article  CAS  PubMed  Google Scholar 

  129. Mei Y et al (2018) Nucleocytoplasmic shuttling of geminivirus C4 protein mediated by phosphorylation and myristoylation is critical for viral pathogenicity. Mol Plant 11(12):1466–1481. https://doi.org/10.1016/j.molp.2018.10.004

    Article  CAS  PubMed  Google Scholar 

  130. Mei Y, Zhang F, Wang M, Li F, Wang Y, Zhou X (2020) Divergent Symptoms caused by geminivirus-encoded C4 proteins correlate with their ability to bind NbSKη. J Virol 94(20):1–12. https://doi.org/10.1128/jvi.01307-20

    Article  CAS  Google Scholar 

  131. Clouse SD (2002) Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. Mol Cell 10(5):973–982. https://doi.org/10.1016/S1097-2765(02)00744-X

    Article  CAS  PubMed  Google Scholar 

  132. Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64(9):2541–2555. https://doi.org/10.1093/jxb/ert080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Weijers D, Wagner D (2016) Transcriptional responses to the auxin hormone. Annu Rev Plant Biol 67(February):539–574. https://doi.org/10.1146/annurev-arplant-043015-112122

    Article  CAS  PubMed  Google Scholar 

  134. Padmanabhan MS, Kramer SR, Wang X, Culver JN (2008) Tobacco mosaic virus replicase-auxin/indole acetic acid protein interactions: reprogramming the auxin response pathway to enhance virus infection. J Virol 82(5):2477–2485. https://doi.org/10.1128/jvi.01865-07

    Article  CAS  PubMed  Google Scholar 

  135. Padmanabhan MS, Goregaoker SP, Golem S, Shiferaw H, Culver JN (2005) Interaction of the tobacco mosaic virus replicase protein with the Aux/IAA protein PAP1/IAA26 is associated with disease development. J Virol 79(4):2549–2558. https://doi.org/10.1128/jvi.79.4.2549-2558.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Jin L et al (2016) Rice Dwarf Virus P2 protein Hijacks auxin signaling by directly targeting the rice OsIAA10 protein, enhancing viral infection and disease development. PLoS Pathog 12(9):1–23. https://doi.org/10.1371/journal.ppat.1005847

    Article  CAS  Google Scholar 

  137. Zhang H et al (2019) Suppression of auxin signalling promotes rice susceptibility to rice black streaked dwarf virus infection. Mol Plant Pathol 20(8):1093–1104. https://doi.org/10.1111/mpp.12814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors acknowledge the financial assistance received from J. C. Bose Fellowship, Science and Engineering Research Board, Government of India to ID (SB/S2/JCB-057/2016). KG acknowledges the fellowship from the Department of Science and Technology (DST), Government of India under Innovation in Science Pursuit for Inspired Research (INSPIRE; grant number DST/INSPIRE Fellowship/2015/IF150761) Faculty Research Program Grant under IoE, University of Delhi.

Funding

F.unding was received from J. C. Bose Fellowship, Science and Engineering Research Board, Government of India to ID (SB/S2/JCB-057/2016), Faculty Research Program Grant under IoE, University of Delhi and the Fellowship from the Department of Science and Technology, Government of India under Innovation in Science Pursuit for Inspired Research (INSPIRE; grant number DST/INSPIRE Fellowship/2015/IF150761) to KG.

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Authors and Affiliations

  1. Department of Plant Molecular Biology, University of Delhi South Campus, New Delhi, -110021, India

    Kanika Gupta & Indranil Dasgupta

  2. Department of Botany, Bhagat Singh Government P.G. College, Jaora, Ratlam, Madhya Pradesh, 457226, India

    Rashmi Rishishwar

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  1. Kanika Gupta
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KG, RR and ID conceptualized the review; KG and RR performed the data analysis and prepared the original draft of the manuscript; ID edited the manuscript and arranged the funding.

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Correspondence to Indranil Dasgupta.

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Gupta, K., Rishishwar, R. & Dasgupta, I. The interplay of plant hormonal pathways and geminiviral proteins: partners in disease development. Virus Genes 58, 1–14 (2022). https://doi.org/10.1007/s11262-021-01881-6

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