Abstract
Cowpea aphid-borne mosaic virus (CABMV) is the main pathogen that affects passion fruit, causing woodiness disease in Brazil. The identification of sources of resistance in Passiflora is necessary for the development of resistant cultivars. The objective of this work was to evaluate the reaction of eight species of Passiflora to CABMV and to verify leaf anatomical changes caused by CABMV. Inoculations were performed and symptoms were evaluated until 55 days after inoculation using a scale ranging from 1 (without symptoms) to 4 (highly susceptible). Simultaneously, leaves from infected and control plants for anatomical analysis were collected. The severity of the disease was calculated using the disease index (DI%) and the means were grouped using the Scott-Knott test. The wild species Passiflora malacophylla, P. setacea and P. suberosa were classified as resistant to CABMV. In contrast, P. alata and P. edulis were susceptible to the virus, with DI values of 58.2 and 51.9%, respectively. Leaf anatomical changes were more drastic in P. edulis and P. alata. In P. edulis, the infection resulted in changes in the organization of the vascular bundles. Resistant wild species showed few anatomical changes. The resistance found in wild species opens the prospect of performing interspecific crosses.
Similar content being viewed by others
References
Alexander MM, Cilia M (2016) A molecular tug-of-war: global plant proteome changes during viral infection. Curr Plant Biol 5:13–24. https://doi.org/10.1016/j.cpb.2015.10.003
Andersen EJ, Ali S, Byamukama E, Yen Y, Nepal MP (2018) Disease resistance mechanisms in plants. Genes 9:1–30. https://doi.org/10.3390/genes9070339
Bolton MD (2009) Primary metabolism and plant defense: fuel for the fire. Mol Plant Microbe Interact 22:487–449. https://doi.org/10.1094/MPMI-22-5-0487
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. https://doi.org/10.1146/annurev-phyto-080614-120106
Cai Y, Cai X, Wang Q, Wang P, Zhang Y, Cai C, Geng S (2020) Genome sequencing of the australian wild diploid species Gossypium australe highlights disease resistance and delayed gland morphogenesis. Plant Biotechnol J 18:814–828. https://doi.org/10.1111/pbi.13249
Carvalho BM, Viana AP, Santos PHD, Generoso AL, Corrêa CCG, Silveira V, Santos EA (2019) Proteome of resistant and susceptible Passiflora species in the interaction with Cowpea aphid-borne mosaic virus reveals distinct responses to pathogenesis. Euphytica 215:1–17. https://doi.org/10.1007/s10681-019-2491-5
Chen XY, Kim JY (2009) Callose synthesis in higher plants. Plant Signal Behav 4:489–492. https://doi.org/10.4161/psb.4.6.8359
El-Banna OHM, Awad MA, Abbas MS, Waziri HM, Darwish HS (2014) Anatomical and ultrastructural changes in tomato and grapevine leaf tissues infected with tomato ringspot virus. Egyptian J Virol 11:102–111
Ellinger D, Voigt CA (2014) The use of nanoscale fluorescence microscopic to decipher cell wall modifications during fungal penetration. Front Plant Sci 5:1–6. https://doi.org/10.3389/fpls.2014.00270
Fernández-Calvino L, Osorio S, Hernández ML, Hamada IB, Del Toro FJ, Donaire L, Yu A, Bustos R, Fernie AR, Martínez-Rivas JM, Llave C (2014) Virus-induced alterations in primary metabolism modulate susceptibility to Tobacco rattle virus in Arabidopsis. Plant Physiol 166:1821–1838. https://doi.org/10.1104/pp.114.250340
Freitas JCO, Viana AP, Santos EA, Silva FH, Paiva CL, Rodrigues R, Souza MM, Eiras M (2015) Genetic basis of the resistance of a passion fruit segregant population to Cowpea aphid borne mosaic virus (CABMV). Trop Plant Pathol 40:291–297. https://doi.org/10.1007/s40858-015-0048-2
Freitas JCO, Viana AP, Santos EA, Paiva CL, Silva FHL, Souza MM (2016) Sour passion fruit breeding: Strategy applied to individual selection in segregating population of Passiflora resistant to Cowpea aphid-born mosaic virus (CABMV). Sci Hortic 211:241–247. https://doi.org/10.1016/j.scienta.2016.09.002
Garcêz RM, Chaves ALR, Eiras M, Meletti LMM, Azevedo Filho JA, Silva LA, Colariccio A (2015) Survey of aphid population in a yellow passion fruit crop and its relationship on the spread Cowpea aphid borne mosaic virus in a subtropical region of Brazil. Springerplus 4:1–12. https://doi.org/10.1186/s40064-015-1263-5
Gomes RT, Kitajima EW, Tanaka FAO, Marques JPR, Appezzato-Glória B (2010) Anatomia de lesões foliares causadas pelo vírus da Mancha Clorótica do Clerodendrum, transmitido pelo ácaro Brevipalpus phoenicis em diferentes espécies. Summa Phytopathol 36:291–297. https://doi.org/10.1590/S0100-54052010000400003
Gonçalves ZS, Lima LKS, Soares TL, Abreu EFM, Barbosa CJ, Cerqueira-Silva CBM, Jesus ON, Oliveira EJ (2018) Identification of Passiflora spp. genotypes resistant to Cowpea aphid-borne mosaic virus and leaf anatomical response under controlled conditions. Sci Hortic 231:166–178. https://doi.org/10.1016/j.scienta.2017.12.008
Gouveia BC, Calil IP, Machado JPB, Santos AA, Fontes EP (2017) Immune receptors and co-receptors in antiviral innate immunity in plants. Front Microbiol 7:1–14. https://doi.org/10.3389/fmicb.2016.02139
Grove J, Marsh M (2011) The cell biology of receptor-mediated virus entry. J Cell Biol 195:1071–1082. https://doi.org/10.1083/jcb.201108131
Hinch JM, Clarke AE (1982) Callose formation in Zea mays as a response to infection with Phytophthora cinnamomi. Physiol Plant Pathol 21:113–124. https://doi.org/10.1016/0048-4059(82)90014-5
IBGE - Instituto Brasileiro de Geografia e Estatística (2020) Survey of national passion fruit production in the year 2018. https://sidra.ibge.gov.br/tabela/5457/. Accessed 18 Mar 2020
Jesus ON, Soares TL, Oliveira EJ, Santos TCP, Farias DH, Bruckner CH, Novaes QS (2016) Dissimilarity based on morphological characterization and evaluation of pollen viability and in vitro germination in Passiflora hybrids and backcrosses. Acta Hortic 29:401–408. https://doi.org/10.17660/ActaHortic.2016.1127.62
KitajimA EW, Alcantara BK, Madureira PM, Alfenas-Zerbini P, Rezende JAM, Zerbini FM (2008) A mosaic of beach bean (Canavalia rosea) caused by an isolate of Cowpea aphid-borne mosaic virus (CABMV) in Brazil. Arch Virol 153:743–747. https://doi.org/10.1007/s00705-008-0052-7
Kraus JR, Arduin M (1997) Basic manual of methods in plant morphology. Eduar, Rio de Janeiro
Lima LKS, Jesus ON, Soares TL, Oliveira SAS, Haddad F, Girardi EA (2019) Water deficit increases the susceptibility of yellow passion fruit seedlings to Fusarium wilt in controlled conditions. Sci Hortic 243:609–621. https://doi.org/10.1016/j.scienta.2018.09.017
Lima LKS, Jesus ON, Soares TL, Santos IS, Oliveira EJ, Coelho Filho MA (2020) Growth, physiological, anatomical and nutritional responses of two phenotypically distinct passion fruit species (Passiflora L.) and their hybrid under saline conditions. Sci Hortic 263:2–15. https://doi.org/10.1016/j.scienta.2019.109037
Mckinney HH (1923) Influence of soil temperature and moisture on infection of wheat seedlings by Helminthosporium sativum. J Agric Res 26:195–218
Meletti LMM, Soares-Scott MD, Bernacci LC, Passos IRS (2005) Melhoramento genético do maracujá: passado e futuro. In: Faleiro FG, Junqueira NTV, Braga MF (eds) Maracujá: germoplasma e melhoramento genético. Embrapa Cerrados, Planaltina, pp 55–78
Melo CAF, Souza MM, Viana AP, Santos EA, Oliveira Souza V, Corrêa RX (2016) Morphological characterization and genetic parameter estimation in backcrossed progenies of Passiflora L. for ornamental use. Sci Hortic 212:91–103. https://doi.org/10.1016/j.scienta.2016.08.013
Murray RR, Emblow MS, Hetherington AM, Foster GD (2016) Plant virus infections control stomatal development. Sci Rep 6:1–7. https://doi.org/10.1038/srep34507
Netherton CL, Wileman T (2011) Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr Opin Virol 1:381–387. https://doi.org/10.1016/j.coviro.2011.09.008
Niehl A, Heinlein M (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248:75–99. https://doi.org/10.1007/s00709-010-0246-1
Novaes QS, Rezende JAM (2003) Selected mild strains of Passion fruit woodiness virus (PWV) fail to protect preimmunized vines in Brazil. Sci Agric 60:699–708. https://doi.org/10.1590/S0103-90162003000400014
Oliveira EJ, Soares TL, Barbosa CDJ, Santos-Filho HP, Jesus ON (2013) Disease severity from passion fruit to identify sources of resistance in field conditions. Rev Bras Frut 35:485–492. https://doi.org/10.1590/S0100-29452013000200018
Palomares-Rius JE, Escobar C, Cabrera J, Vovlas A, Castilla P (2017) Anatomical alterations in plant tissues induced by plant-parasitic Nematodes. Front Plant Sci 8:1–16. https://doi.org/10.3389/fpls.2017.01987
Pamponét VCC, Souza MM, Silva GS, Micheli F, Melo CAF, Oliveira SG, Corrêa RX (2019) Low coverage sequencing for repetitive DNA analysis in Passiflora edulis Sims: citogenomic characterization of transposable elements and satellite DNA. BMC Genomics 262:1–17. https://doi.org/10.1186/s12864-019-5576-6
Preisigke SDC, Viana AP, Santos EA, Santos PRD, Santos VOD, Ambrósio M, Walter FHDB (2020) Selection strategies in a segregating passion fruit population aided by classic and molecular techniques. Bragantia 79:1–15. https://doi.org/10.1590/1678-4499.20190291
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rai AK, Basavaraj YB, Sadashiva AT, Krishna M, Reddy M, Ravishankar KV, Hussain Z, Venugopalan R, Reddy MK (2020) Evaluation of tomato genotypes for resistance to bud necrosis disease caused by groundnut bud necrosis virus (GBNV). Crop Prot 131:1–8. https://doi.org/10.1016/j.cropro.2019.105074
Rasband WS (2016) ImageJ. U S National Institutes of Health, Bethesda
Sacoman NN, Viana AP, Carvalho VS, Santos EA, Rodrigues R (2018) Resistance to Cowpea aphid-borne mosaic virus in in vitro germinated genotypes of Passiflora setacea. Rev Bras Frut 40:1–10. https://doi.org/10.1590/0100-29452017607
Sade D, Sade N, Brotman Y, Czosnek H (2020) Tomato yellow leaf curl virus (TYLCV)-resistant tomatoes share molecular mechanisms sustaining resistance with their wild progenitor Solanum habrochaites but not with TYLCV-susceptible tomatões. Plant Sci 110439:1–6. https://doi.org/10.1016/j.plantsci.2020.110439
Santos EA, Viana AP, Freitas JCO, Rodrigues DL, Ferreira RT, Paiva CL, Souza MM (2015b) Genotype selection by REML/BLUP methodology in a segregating population from an interspecific Passiflora spp. crossing. Euphytica 204:1–11. https://doi.org/10.1007/s10681-015-1367-6
Santos EA, Viana AP, Oliveira FJC, Lima FH, Rodrigues RAND, Eiras M (2015a) Resistance to Cowpea aphid borne mosaic virus in species and hybrids of Passiflora: advances for the control of the passion fruit woodiness disease in Brazil. Eur J Plant Pathol 143:85–98. https://doi.org/10.1007/s10658-015-0667-y
Santos VOD, Viana AP, Preisigke SDC, Santos EA (2019) Characterization of a segregating population of passion fruit with resistance to Cowpea aphid borne mosaic virus through morpho-agronomic descriptors. Gen Mol Res 18:1–13. https://doi.org/10.4238/gmr18255
Soares TL, Jesus ON, Souza EHAND, Oliveira EJ (2015) Reproductive biology and pollen–pistil interactions in Passiflora species with ornamental potential. Sci Hortic 197:339–349. https://doi.org/10.1016/j.scienta.2015.09.045
Soares TL, Jesus ON, Souza EH, Oliveira EJ (2018) Floral development stage and its implications for the reproductive success of Passiflora L. Sci Hortic 238:333–342. https://doi.org/10.1016/j.scienta.2018.04.034
Souza MM, Pereira TNS, Silva LC, Reis DSS, Sudré CP (2003) Karyotype of six Passiflora species collected in the state of Rio de Janeiro. Cytologia 68:165–171. https://doi.org/10.1508/cytologia.68.165
Souza PU, Lima LKS, Soares TL, Jesus ON, Coelho Filho MA, Girardi EA (2018) Biometric, physiological and anatomical responses of Passiflora spp. to controlled water deficit. Sci Hortic 229:77–90. https://doi.org/10.1016/j.scienta.2017.10.019
Spadotti DMDA, Favara GM, Novaes QS, Mello APOA, Freitas DMS, Edwards Molina JPAND, Rezende JAM (2019) Long lasting systematic roguing for effective management of CABMV in passion flower orchards through maintenance of separated plants. Plant Pathol 68:1259–1267. https://doi.org/10.1111/ppa.13054
Su J, Yang L, Zhu Q, Wu H, He Y, Liu Y, Zhang S (2018) Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity. PLoS Biol 16:1–29. https://doi.org/10.1371/journal.pbio.2004122
Takimoto JK, Queiroz-Voltan RB, Souza-Dias JACD, Cia E (2009) Alterações anatômicas em algodoeiro infectado pelo vírus da doença azul. Bragantia 68:109–116. https://doi.org/10.1590/S0006-87052009000100012
Xiao Y, Tholen D, Zhu XG (2016) The influence of leaf anatomy on the internal light environment and photosynthetic electron transport rate: exploration with a new leaf ray tracing model. J Exp Bot 67:6021–6035. https://doi.org/10.1093/jxb/erw359
Xiao D, Duan X, Zhang M, Sun T, Sun X, Li F, Wang D (2018) Changes in nitric oxide levels and their relationship with callose deposition during the interaction between soybean and soybean mosaic virus. Plant Biol 20:318–326. https://doi.org/10.1111/plb.12663
Acknowledgements
The Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) provided a doctoral research grant to the first author (Z.S.G) and postdoctoral research grants to the third author (T.L.S – PNPD/UEFS 15950830814) and fourth author (E.H.S – PNPD 88882.315208/2019-01). The Conselho Nacional de Desenvolvimento Ciêntífico e Tecnológico (CNPq) provided a postdoctoral scholarship to the second author (L.K.S.L – PDJ 152109/2019-6), financial support (Process 421033/2018-5) and a research productivity fellowship to the fifth author (O.N.J. – PQ312774/2018-4). The Embrapa Mandioca e Fruticultura research unit provided the plant material along with experimental, technical and financial support (Process 22.16.04.007.00.00). Professor Elliot Watanabe Kitajima and the Nucleus for Electronic Microscopy of the Universidade de São Paulo (Esalq-USP) supported the processing of samples for transmission electron microscopy.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Electronic supplementary material
ESM 1
(DOCX 1.12 MB)
Rights and permissions
About this article
Cite this article
Gonçalves, Z.S., Lima, L.K.S., Soares, T.L. et al. Leaf anatomical aspects of CABMV infection in Passiflora spp. by light and fluorescence microscopy. Australasian Plant Pathol. 50, 203–215 (2021). https://doi.org/10.1007/s13313-020-00763-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13313-020-00763-z