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RESEARCH ARTICLE
Contents Vol 59(12)

Histopathology comparison and phenylalanine ammonia lyase (PAL) gene expressions in Fusarium wilt infected watermelons

P.-F. L. Chang A C , C.-C. Hsu A , Y.-H. Lin A , K.-S. Chen B , J.-W. Huang A and T.-D. Liou B
+ Author Affiliations
- Author Affiliations

A Department of Plant Pathology, National Chung Hsing University, Taichung, Taiwan 402, R.O.C.

B Fengshan Tropical Horticultural Experiment Branch, Agricultural Research Institute, Council of Agriculture, Fengshan, Kaohsiung, Taiwan 830, R.O.C.

C Corresponding author. Email: pfchang@nchu.edu.tw

Australian Journal of Agricultural Research 59(12) 1146-1155 https://doi.org/10.1071/AR08066
Submitted: 20 February 2008  Accepted: 7 October 2008   Published: 10 November 2008

Abstract

Fusarium wilt disease of watermelon (Citrullus lanatus (Thunb.) Matsum & Nakai), caused by Fusarium oxysporum f. sp. niveum (FON), is one of the limiting factors of worldwide watermelon production. In this study, a Fusarium wilt resistant watermelon JSB, which was derived from a spontaneous mutation of the susceptible Sugar Baby (SB), was used to investigate histopathology. The number and diameter of xylem vessels in the root (10 mm below the shoot base) of resistant JSB plants were significantly higher than those in susceptible SB plants. At 9 days post inoculation (dpi), using the plate assay on Nash-PCNB media, FON could be recovered from 86% of the roots in the symptomless plants of both watermelon lines, and from 55% and 64% of the stem segments (5 mm above the shoot base) in resistant and susceptible plants, respectively. In paraffin and free-hand tissue sections, at 8, 13, and 35 dpi, the xylem of roots and stems close to the soil surface in resistant watermelon JSB plants was also colonised by FON, but to a much lower percentage than the susceptible SB ones. No colonisation below the middle of stems was observed in the resistant JSB plants. The susceptible plants grown in infested soil were all dead by 35 dpi, while the resistant plants remained healthy. These observations suggest that reducing FON colonisation in the vascular systems of the host may contribute to the resistance in JSB. Furthermore, the higher expression of the phenylalanine ammonia lyase (PAL) gene in JSB induced by FON and the effects of PAL inhibitor on the resistance of JSB suggested that PAL is involved in resistance of watermelon to Fusarium wilt pathogen.

Additional keywords: watermelon, Fusarium oxysporum f. sp. niveum, resistance mechanism, xylem, plant histopathology.


Acknowledgments

The authors thank Dr S.-J. Hsiao (National Chung Hsing University, Taiwan) for her technical support in paraffin cross- and free-hand sectioning. We are grateful to Drs W. H. Ko (National Chung Hsing University, Taiwan) and Gad Loebenstein (The Agricultural Research Organization of Israel) for critical reading and suggestions on this manuscript. This research was supported in part by grants: 90AS-2.1.2-BQ-B7, NSC 91-2313-B-005-094, NSC 92-2313-B-005-054, and NSC 93-2313-B-005-080; by the Ministry of Education, Taiwan, R.O.C., under the ATU plan; and by the National Chung Hsing University.


References


Baayen RP (1986) Regeneration of vascular tissues in relation to Fusarium wilt resistance of carnation. Netherlands Journal of Plant Pathology 92, 273–285.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Baayen RP, van Eijk C, Elgersma DM (1989) Histology of roots of resistant and susceptible carnation cultivars from soil infested with Fusarium oxysporum f. sp. dianthi. Netherlands Journal of Plant Pathology 95, 3–13.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Bell AA , Mace ME (1981) Biochemistry and physiology of resistance. In ‘Fungal wilt diseases of plants’. (Eds ME Mace, AA Bell, CH Beckman) pp. 431–438. (Academic Press: New York)

Ben-Yephet Y, Reuven M, Shtienberg D (1997) Complete resistance by carnation cultivars to Fusarium wilt induced by Fusarium oxysporum f. sp. dianthi race 2. Plant Disease 81, 777–780.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Bucciarelli B, Jung HG, Ostry ME, Anderson NA, Vance CP (1998) Wound response characteristics as related to phenylpropanoid enzyme activity and lignin deposition in resistant and susceptible Populus tremuloides inoculated with Entoleuca mammata (Hypoxylon mammatum). Canadian Journal of Botany 76, 1282–1289.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Cahill DM, McComb JA (1992) A comparison of changes in phenylalanine ammonia-lyase activity, lignin and phenolic synthesis in the roots of Eucalyptus calophylla (field resistant) and E. marginata (susceptible) when infected with Phytophthora cinnamomi. Physiological and Molecular Plant Pathology 40, 315–332.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. The Plant Cell 6, 1583–1592.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Carver TLW, Zhang L, Zeyen RJ, Robbins MP (1996) Phenolic biosynthesis inhibitors suppress adult plant resistance to Erysiphe graminis in oat at 20°C and 10°C. Physiological and Molecular Plant Pathology 49, 121–141.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chandra A, Saxena R, Dubey A, Saxena P (2007) Change in phenylalanine ammonia lyase activity and isozyme patterns of polyphenol oxidase and peroxidase by salicylic acid leading to enhance resistance in cowpea against Rhizoctonia solani. Acta Physiologiae Plantarum 29, 361–367.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chen KS (2004) Breeding for resistance of watermelon varieties to Fusarium wilt and their genetics analysis of inheritance. Doctoral Dissertation, Department of Plant Pathology, National Chung Hsing University, Taichung, Taiwan, R.O.C.

Chen KS, Chang PFL, Liou TD, Huang JW (2003a) Identification of physiological races of Fusarium oxysporum f. sp. niveum and breeding for Fusarium wilt-resistant watermelon line. Plant Pathology Bulletin 12, 247–254. open url image1

Chen KS, Liou TD, Chang PFL, Huang JW (2003b) Selection for resistance of watermelon varieties (lines) to Fusarium wilt and their genetic analysis of inheritance. Plant Pathology Bulletin 12, 173–180. open url image1

Clark TA, Zeyen RJ, Smith AG, Carver TLW, Vance CP (1994) Phenylalanine ammonia lyase mRNA accumulation, enzyme activity and cytoplasmic responses in barley isolines, differing at MI-a and MI-o loci, attacked by Erysiphe graminis f. sp. hordei. Physiological and Molecular Plant Pathology 44, 171–185.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

COA (2006) ‘COA yearbook’. (Council of Agriculture, Executive Yuan, Annal Report of Agricultural Statistics: Taipei, Taiwan, R.O.C.)

Corchete MP, Diez JJ, Valle T (1993) Phenylalanine ammonia-lyase activity in suspension cultures of Ulmus pumila and U. campestris treated with spores of Ceratocystis ulmi. Plant Cell Reports 13, 111–114.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Cui Y, Bell AA, Joost O, Magill C (2000) Expression of potential defense response genes in cotton. Physiological and Molecular Plant Pathology 56, 25–31.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Cui Y, Magill J, Frederiksen R, Magill C (1996) Chalcone synthase and phenylalanine ammonia-lyase mRNA levels following exposure of sorghum seedlings to three fungal pathogens. Physiological and Molecular Plant Pathology 49, 187–199.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Curir P, Dolci M, Galeotti F (2005) A phytoalexin-like flavonol involved in the carnation (Dianthus caryophyllus)-Fusarium oxysporum f. sp. dianthi pathosystem. Journal of Phytopathology 153, 65–67.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

De Ascensao ARDCF, Dubery IA (2000) Panama disease: cell wall reinforcement in banana roots in response to elicitors from Fusarium oxysporum f. sp. cubense race four. Phytopathology 90, 1173–1180.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

De Cal A, Garcia-Lepe R, Melgarejo P (2000) Induced resistance by Penicillium oxalicum against Fusarium oxysporum f. sp. lycopersici: histological studies of infected and induced tomato stems. Phytopathology 90, 260–268.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dixon RA, Harrison MJ, Lamb CJ (1994) Early events in the activation of plant defense responses. Annual Review of Phytopathology 32, 479–501.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Duan XH, Yh Yu, Bin JH (2004) Effects of aminoxyacetic acid (AOA) and 2-aminoindan-2-phosphonic acid (AIP) on the activities of some enzymes induced by methyl jasmonate in tobacco calli. Journal of Tropical and Subtropical Botany 12, 345–350.
|  CAS |
open url image1

FAO (2006) ‘FAO yearbook (production).’ (Food and Agriculture Organization of the United Nations: Rome)

Hahlbrock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 40, 347–369.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

He C, Hsiang T, Wolyn DJ (2001) Activation of defense responses to Fusarium infection in Asparagus densiflorus. European Journal of Plant Pathology 107, 473–483.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Hsu CC (2005) Distribution of Fusarium oxysporum f. sp. niveum and expression of the defense-related genes in inoculated resistant and susceptible watermelon plants. Master’s Thesis, Department of Plant Pathology, National Chung Hsing University, Taichung, Taiwan, R.O.C.

Huang JW (1978) The biology of Fusarium oxysporum f. sp. niveum, the causal agent of watermelon wilt, and control of the disease in the field. Master’s Thesis, Department of Plant Pathology, National Chung Hsing University, Taichung, Taiwan, R.O.C.

Huertas-González MD, Ruiz-Roldán MC, Di Pietro A, Roncero MIG (1999) Cross protection provides evidence for race-specific avirulence factors in Fusarium oxysporum. Physiological and Molecular Plant Pathology 54, 63–72.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Jiang YR, Fang WP, Zhu SJ, Ji DF (2005) Relationship of verticillium wilt resistance with plant anatomical structure and biochemical metabolism in upland cotton. Acta Agronomica Sinica 31, 337–341.
|  CAS |
open url image1

Johansen DA (1940) ‘General methods (Section I), Plant microtechnique. Ch. VI: Stains.’ pp. 59–62. (McGraw-Hill Book Company, Inc.: New York)

Jones DH (1984) Phenylalanine ammonia-lyase: regulation of its induction, and its role in plant development. Phytochemistry 23, 1349–1359.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kruger WM, Szabo LJ, Zeyen RJ (2003) Transcription of the defense response genes chitinase IIb, PAL and peroxidase is induced by the barley powdery mildew fungus and is only indirectly modulated by R genes. Physiological and Molecular Plant Pathology 63, 167–178.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kuhn DN, Chappell J, Boudet A, Hahlbrock K (1984) Induction of phenylalanine ammonia-lyase and 4-coumarate CoA ligase mRNAs in cultured plant cells by UV light or fungal elicitor. Proceedings of the National Academy of Sciences of the United States of America 81, 1102–1106.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lin KC, Bushnell WR, Smith AG, Szabo LJ (1998) Temporal accumulation patterns of defense response gene transcripts in relation to resistant reactions in oat inoculated with Puccinia graminis. Physiological and Molecular Plant Pathology 52, 95–114.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lozovaya VV, Lygin AV, Li S, Hartman GL, Widholm JM (2004) Biochemical response of soybean roots to Fusarium solani f. sp. glycines infection. Crop Science 44, 819–826.
|  CAS |
open url image1

Martyn RD, Biles CL, Dillard EA (1991) Induced resistance to Fusarium wilt of watermelon under simulated field condition. Plant Disease 75, 874–877. open url image1

Martyn RD, Netzer D (1991) Resistance to races 0, 1, and 2 of Fusarium wilt of watermelon in Citrullus sp. PI-296341-FR. HortScience 26, 429–432. open url image1

Mauch-Mani B, Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. The Plant Cell 8, 203–212.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Mazeyrat F, Mouzeyar S, Courbou I, Badaoui S, Roeckel-Drevet P, Tourvieille de Labrouhe D, Ledoigt G (1999) Accumulation of defense related transcripts in sunflower hypocotyls (Helianthus annuus L.) infected with Plasmopara halstedii. European Journal of Plant Pathology 105, 333–340.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Moerschbacher BM, Noll U, Gorrichon L, Reisener HJ (1990) Specific inhibition of lignification breaks hypersensitive resistance of wheat to stem rust. Plant Physiology 93, 465–470.
|  CAS | PubMed |
open url image1

Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous gene in trans. The Plant Cell 2, 279–289.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Nash SM, Snyder WC (1962) Quantitative estimations by plate counts of propagules of the bean root rot Fusarium in field soils. Phytopathology 52, 567–572. open url image1

Prats E, Bazzalo ME, León A, Jorrín JV (2003) Accumulation of soluble phenolic compounds in sunflower capitula correlates with resistance to Sclerotinia sclerotiorum. Euphytica 132, 321–329.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Reisener HJ , Tiburzy R , Kogel KH , Moerschbacher B , Heck B (1986) Mechanism of resistance of wheat against stem rust in the Sr5/P5 interaction. In ‘Biology and molecular biology of plant–pathogen interactions’. (Ed. JA Bailey) pp. 141–148. (Springer-Verlag: Berlin)

Shadle GL, Wesley SV, Korth KL, Chen F, Lamb C, Dixon RA (2003) Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of L-phenylalanine ammonia-lyase. Phytochemistry 64, 153–161.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Shah J (2003) The salicylic acid loop in plant defense. Current Opinion in Plant Biology 6, 365–371.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Smith CJ (1996) Accumulation of phytoalexins: defense mechanisms and stimulus response system. New Phytologist 132, 1–45.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Smith SN (2007) An overview of ecological and habitat aspects in the genus Fusarium with special emphasis on the soil-borne pathogenic forms. Plant Pathology Bulletin 16, 97–120. open url image1

Solla A, Gil L (2002) Xylem vessel diameter as a factor in resistance of Ulmus minor to Ophiostoma novo-ulmi. Forest Pathology 32, 123–130.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Stadnik MJ, Buchenauer H (2000) Inhibition of phenylalanine ammonia-lyase suppresses the resistance induced by benzothiadiazole in wheat to Blumeria graminis f. sp. tritici. Physiological and Molecular Plant Pathology 57, 25–34.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Takahashi H, Takita K, Kishimoto T, Mitsui T, Hori H (2002) Ca2+ is required by clubroot resistant turnip cells for transient increases in PAL activity that follow inoculation with Plasmodiophora brassicae. Journal of Phytopathology 150, 529–535.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tsai SH (2002) ‘Plant anatomy.’ (National Institute for Compilation and Translation: Taipei, Taiwan, R.O.C.)

Vakalounakis DJ, Wang Z, Fragkiadakis GA, Skaracis GN, Li DB (2004) Characterization of Fusarium oxysporum isolates obtained from cucumber in China by pathogenicity, VCG, and RAPD. Plant Disease 88, 645–649.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Way HM, Kazan K, Mitter N, Goulter KC, Birch RG, Manners JM (2002) Constitutive expression of a phenylalanine ammonia-lyase gene from Stylosanthes humilis in transgenic tobacco leads to enhanced disease resistance but impaired plant growth. Physiological and Molecular Plant Pathology 60, 275–282.
|  CAS |
open url image1

Zhou XG, Everts KL (2004) Quantification of root and stem colonization of watermelon by Fusarium oxysporum f. sp. niveum and its use in evaluating resistance. Phytopathology 94, 832–841.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1