Abstract
Genetic resistance is the main strategy to control Fusarium wilt in common bean. Despite this, few studies have focused on defense mechanisms involved in bean resistance to Fusarium oxysporum f. sp. phaseoli (Fop). Thus, the present study aimed to investigate the changes in xylem morphology and involvement of phenylpropanoid compounds and their biosynthetic enzymes in bean resistance against Fop. Uirapuru and UFSC-01 genotypes characterized, respectively, as susceptible and resistant were used. In roots and hypocotyls, guaiacol peroxidase (GPX), phenylalanine ammonia-lyase (PAL), and polyphenol oxidase (PPO) activities were determined at 0, 1, 2, 3, 4, 5, and 6 days after inoculation (dai), and flavonoids, total phenolics, and lignin content were quantified at 0, 3, and 6 dai. Cross sections of taproots and hypocotyls were examined under epifluorescence (at 1, 3, and 6 dai) and transmission electron (at 6 dai) microscopic to analyze the morphology of xylem cell walls. Overall, there was an increase in the activity of all studied enzymes in resistant bean plants, mainly during advanced colonization stages. Modifications in xylem morphology were more intense in roots of resistant genotype resulting in an increase of occluded cells, organelles, and cell wall strengthening. This study provides evidence that bean resistance is associated with increased phenylpropanoid enzymatic activity and cell wall reinforcement of some xylem cells.
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References
Alves-Santos FM, Cordeiro-Rodrigues L, Sayagués JM, Martín-Domínguez R, García-Benavides P, Crespo MC, Díaz-Mínguez JM, Eslava AP (2002) Pathogenicity and race characterization of Fusarium oxysporum f. sp. phaseoli isolates from Spain and Greece. Plant Pathol 51:605–611. https://doi.org/10.1046/j.1365-3059.2002.00745.x
Arfaoui A, El Hadrami A, Mabrouk Y, Sifi B, Boudabous A, El Hadrami I, Daayf F, Chérif M (2007) Treatment of chickpea with Rhizobium isolates enhances the expression of phenylpropanoid defense-related genes in response to infection by Fusarium oxysporum f. sp. ciceris. Plant Physiol Biochem 45:470–479. https://doi.org/10.1016/j.plaphy.2007.04.004
Baayen RP, Elgersma DM (1985) Colonization and histopathology of susceptible and resistant carnation cultivars infected with Fusarium oxysporum f. sp. dianthi. Neth J Plant Pathol 91:119–135. https://doi.org/10.1007/BF01976386
Bani M, Pérez-De-Luque A, Rubiales D, Rispail N (2018) Physical and chemical barriers in root tissues contribute to quantitative resistance to Fusarium oxysporum f. sp. pisi in pea. Front Plant Sci 9:199. https://doi.org/10.3389/fpls.2018.00199
Beckman CH (1987) The nature of wilt diseases of plants. APS press, St. Paul, Minn. p 175
Block A, Li G, Fu ZQ, Alfano JR (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11:396–403. https://doi.org/10.1016/j.pbi.2008.06.007
Bouzon ZL, Ouriques LC, Oliveira EC (2006) Spore adhesion and cell wall formation in Gelidium floridanum (Rhodophyta, Gelidiales). J Appl Psychol 18:287–294. https://doi.org/10.1007/s10811-006-9028-8
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Buruchara RA, Camacho L (2000) Common bean reaction to Fusarium oxysporum f. sp. phaseoli, the cause of severe vascular wilt in Central Africa. J Phytopathol 148:39–45. https://doi.org/10.1046/j.1439-0434.2000.00457.x
Chen L, Wu Q, He W, He T, Wu Q, Miao Y (2019) Combined de novo transcriptome and metabolome analysis of common bean response to Fusarium oxysporum f. sp. phaseoli infection. Int J Mol Sci 20(24):6278. https://doi.org/10.3390/ijms20246278
Chong J, Baltz R, Fritig B, Saindrenan P (1999) An early salicylic acid-, pathogen-and elicitor-inducible tobacco glucosyltransferase: role in compartmentalization of phenolics and H2O2 metabolism. FEBS Let 458:204–208. https://doi.org/10.1016/s0014-5793(99)01154-0
Dayal V (2015) An introduction to R for quantitative economics. Springer, New Delhi, p 109. https://doi.org/10.1007/978-81-322-2340-5
de Borba MC, Garcés-Fiallos FR, Stadnik MJ (2017) Reactions of black bean seedlings and adult plants to infection by Fusarium oxysporum f. sp. phaseoli. Crop Prot 96:221–227. https://doi.org/10.1016/j.cropro.2017.02.019
de Quadros F, Garcés-Fiallos FR, de Borba MC, de Freitas MB, Stadnik MJ (2019) Fusarium oxysporum affects differently the hydrogen peroxide levels and oxidative metabolism in susceptible and resistant bean roots. Physiol Mol Plant P 106:1–9. https://doi.org/10.1016/j.pmpp.2018.11.001
de Quadros FM, de Freitas MB, Simioni C, Ferreira C, Stadnik MJ (2020) Redox status regulation and action of extra-and intravascular defense mechanisms are associated with bean resistance against Fusarium oxysporum f. sp. phaseoli. Protoplasma 257:1457–1472. https://doi.org/10.1007/s00709-020-01521-0
Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MS, Wang L (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Mol Plant Pathol 3:371–390. https://doi.org/10.1046/j.1364-3703.2002.00131.x
El Modafar C, Tantaoui A, El Boustani E (2000) Changes in cell wall-bound phenolic compounds and lignin in roots of date palm cultivars differing in susceptibility to Fusarium oxysporum f. sp. albedinis. J Phytopathol 148:405–411. https://doi.org/10.1046/j.1439-0434.2000.00512.x
Fernandez FO, Gepts PL, López Genes M, Arregocés O (1986) Stages of development of the common bean plant. CIAT, Palmira, p 32
Garcés-Fiallos FR, de Borba MC, Schmidt EC, Bouzon ZL, Stadnik MJ (2017) Delayed upward colonization of xylem vessels is associated with resistance of common bean to Fusarium oxysporum f. sp. phaseoli. Eur J Plant Pathol 149:477–489. https://doi.org/10.1007/s10658-017-1197-6
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
He C, Hsiang T, Wolyn DJ (2001) Activation of defense responses to Fusarium infection in Asparagus densiflorus. Eur J Plant Pathol 107:473–483. https://doi.org/10.1023/A:1011218304331
Hématy K, Cherk C, Somerville S (2009) Host–pathogen warfare at the plant cell wall. Curr Opin Plant Biol 2:406–413. https://doi.org/10.1016/j.pbi.2009.06.007
Jain S, Choudhary DK (2014) Induced defense-related proteins in soybean (Glycine max L. Merrill) plants by Carnobacterium sp. SJ-5 upon challenge inoculation of Fusarium oxysporum. Planta 239:1027–10400. https://doi.org/10.1007/s00425-014-2032-3
Kavino M, Harish S, Kumar N, Saravanakumar D, Samiyappan R (2008) Induction of systemic resistance in banana (Musa spp.) against Banana bunchy top virus (BBTV) by combining chitin with root-colonizing Pseudomonas fluorescens strain CHA0. Eur J Plant Pathol 120:353–362. https://doi.org/10.1007/s10658-007-9223-8
Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335. https://doi.org/10.3390/ijms19020335
Lozovaya VV, Lygin AV, Zernova OV, Li S, Widholm JM, Hartman GL (2006) Lignin degradation by Fusarium solani f. sp. glycines. Plant Dis 90:77–82. https://doi.org/10.1094/PD-90-0077
Mandal S, Mitra A (2007) Reinforcement of cell wall in roots of Lycopersicon esculentum through induction of phenolic compounds and lignin by elicitors. Physiol Mol Plant P 71:4-6. https://doi.org/10.1016/j.pmpp.2008.02.003
Nawrath C (2002) The biopolymers cutin and suberin. The Arabidopsis Book 1:e0021. https://doi.org/10.1199/tab.0021
Niño-Sánchez J, Tello V, Casado-Del Castillo V, Thon MR, Benito EP, Díaz-Mínguez JM (2015) Gene expression patterns and dynamics of the colonization of common bean (Phaseolus vulgaris L.) by highly virulent and weakly virulent strains of Fusarium oxysporum. Front Microbiol 6:234. https://doi.org/10.3389/fmicb.2015.00234
Pereira AC, Cruz MFA, Paula Júnior TJ, Rodrigues FA, Carneiro JES, Vieira RF, Carneiro PCS (2013) Infection process of Fusarium oxysporum f. sp. phaseoli on resistant, intermediate and susceptible bean cultivars. Trop Plant Pathol 38:323–328. https://doi.org/10.1590/S1982-56762013005000022
Pouralibaba HR, Pérez-de-Luque A, Rubiales D (2017) Histopathology of the infection on resistant and susceptible lentil accessions by two contrasting pathotypes of Fusarium oxysporum f. sp. lentis. Eur J Plant Pathol 148:53–63. https://doi.org/10.1007/s10658-016-1068-6
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17(1):208–212. https://doi.org/10.1083/jcb.17.1.208
Schmidt EC, Scariot LA, Rover T, Bouzon ZL (2009) Changes in ultrastructure and histochemistry of two red macroalgae strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a consequence of ultraviolet B radiation exposure. Micron 40(8):860–869. https://doi.org/10.1016/j.micron.2009.06.003
Schuetz M, Smith R, Ellis B (2013) Xylem tissue specification, patterning, and differentiation mechanisms. J Exp Bot 64:11–31. https://doi.org/10.1093/jxb/ers287
Shi J, Mueller WC, Beckman CH (1992) Vessel occlusion and secretory activities of vessel contact cells in resistant or susceptible cotton plants infected with Fusarium oxysporum f. sp. vasinfectum. Physiol Mol Plant Pathol 40:133–147. https://doi.org/10.1016/0885-5765(92)90040-3
Siranidou E, Kang Z, Buchenauer H (2002) Studies on symptom development, phenolic compounds and morphological defence responses in wheat cultivars differing in resistance to Fusarium head blight. J Phytopathol 150:200–208. https://doi.org/10.1046/j.1439-0434.2002.00738.x
Stadnik MJ, Buchenauer H (2000) Inhibition of phenylalanine ammonia-lyase suppresses the resistance induced by benzothiadiazole in wheat to Blumeria graminis f. sp. tritici. Physiol Mol Plant P 57:25–34. https://doi.org/10.1006/pmpp.2000.0276
VanderMolen GE, Beckman CH, Rodehorst E (1987) The ultrastructure of tylose formation in resistant banana following inoculation with Fusarium oxysporum f. sp. cubense. Physiol Mol Plant Pathol 31:185–200. https://doi.org/10.1016/0885-5765(87)90063-4
van Schoonhoven A, Pastor-Corrales MA (1987) Standard system for the evaluation of bean germplasm. Centro Internacional de Agricultura Tropical (CIAT), Cali, p 56
Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, Oxford, p 238
Woisky RG, Salatino A (1988) Analysis of propolis: some parameters and procedures for chemical quality control. J Apic Res 37(2):99–105. https://doi.org/10.1080/00218839.1998.11100961
Wojtasik W, Kulma A, Dymińska L, Hanuza J, Czemplik M, Szopa J (2016) Evaluation of the significance of cell wall polymers in flax infected with a pathogenic strain of Fusarium oxysporum. BMC Plant Biol 16:75. https://doi.org/10.1186/s12870-016-0762-z
Xue R, Wu J, Zhu Z, Wang L, Wang X, Wang S, Blair MW (2015) Differentially expressed genes in resistant and susceptible common bean (Phaseolus vulgaris L.) genotypes in response to Fusarium oxysporum f. sp. phaseoli. PLoS One 10(6):e0127698. https://doi.org/10.1371/journal.pone.0127698
Xue R, Wu X, Wang Y, Zhuang Y, Chen J, Wu J, Ge W, Wang L, Wang S, Blair MW (2017) Hairy root transgene expression analysis of a secretory peroxidase (PvPOX1) from common bean infected by Fusarium wilt. Plant Sci 260:1–7. https://doi.org/10.1016/j.plantsci.2017.03.011
Yadeta KA, Thomma BPHJ (2013) The xylem as battleground for plant hosts and vascular wilt pathogens. Front Plant Sci 4:97. https://doi.org/10.3389/fpls.2013.00097
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FRGF gratefully acknowledges the financial support of the National Secretariat for Higher Education, Science, Technology and Innovation (SENESCYT), Ecuador, and of the Student Program-Covenant Postgraduate (PEC-PG/CAPES), Brazil, by jointly awarded PhD Scholarship. MJS and ZLB are research members of the National Council for Scientific and Technological Development (CNPq).
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FRGF, ZLB, JLBO, and MJS conceived and designed research. FRGF, CF, and FMQ conducted experiments and the analyses. FRGF, FMQ, and MCB contributed new reagents or analytical tools. FRGF and FMQ analyzed data. FRGF, FMQ, and MJS wrote the manuscript. All authors read and approved the manuscript.
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Garcés-Fiallos, F.R., de Quadros, F.M., Ferreira, C. et al. Changes in xylem morphology and activity of defense-related enzymes are associated with bean resistance during Fusarium oxysporum colonization. Protoplasma 259, 717–729 (2022). https://doi.org/10.1007/s00709-021-01691-5
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DOI: https://doi.org/10.1007/s00709-021-01691-5