ارزیابی نقش مسیرهای انتقال سیگنال فنیل پروپانوئید و اکتادکانوئید و برخی از ترکیبات دیواره سلولی مرتبط با دفاع در برهمکنش ارقام گندم با گونه‌های قارچ Fusarium‌

نوع مقاله: مقاله کامل پژوهشی

نویسندگان

1 دانشجوی دکتری گروه گیاه‌پزشکی، دانشکده کشاورزی، دانشگاه فردوسی مشهد، مشهد، ایران

2 دانشیار گروه گیاه‌پزشکی، دانشکده کشاورزی، دانشگاه فردوسی مشهد، مشهد، ایران.

3 استاد گروه گیاه‌پزشکی، دانشکده کشاورزی، دانشگاه فردوسی مشهد، مشهد، ایران.

چکیده

دو گونه قارچ Fusarium graminearum و F. culmorum از عوامل اصلی بیماری بلایت فوزاریومی سنبله گندم در جهان می‌باشند. در حال حاضر، اطلاعات محدودی در مورد مسیرهای سیگنالی دفاعی و مکانیسم‌های درگیر در مقاومت ارقام گندم علیه Fusarium spp. وجوددارد. دو آنزیم فنیل آلانین آمونیالیاز (Phenyl alanine ammonia lyase; PAL) و لیپوکسیژناز (Lipoxygenase; LOX)، به‌عنوان نشانگرهای اصلی مسیرهای انتقال سیگنال فنیل پروپانوئید (phenylpropanoid) و اکتادکانوئید (octadecanoid)، ممکن است در واکنشهای دفاعی در گیاهان نقش داشته باشند. در این پژوهش، فعالیت دو آنزیم PAL و LOX و بیان ژن‌های کد کننده آن‌ها و نیز تولید ترکیبات دفاعی نظیر مواد فنلی و لیگنین در برگ و خوشه دو رقم گندم حساس (فلات) و نسبتاً مقاوم (گاسکوژن) مایه‌زنی شده با دو گونه قارچ F. graminearum و F. culmorum مورد بررسی قرار گرفت. نتایج این تحقیق نشان داد که فعالیت این دو آنزیم و تولید ترکیبات فنلی و لیگنین در برگ و خوشه رقم گاسکوژن در مقایسه با رقم فلات بالاتر است. تجزیه و تحلیل بیان ژن‌های PAL و LOX ارتباط مستقیم بین فعالیت آنزیم‌ها و بیان ژن‌های مربوطه را نشان داد. در اغلب زمان‌های مورد بررسی پس از مایه­زنی، سطوح بالاتری از فعالیت آنزیم‌ها، بیان ژن‌ها و تولید ترکیبات فنلی و لیگنین در تعامل گندم با قارچ F. culmorum مشاهده شد. استفاده از مهارکننده‌های دو آنزیم PAL و LOX  موجب افزایش توسعه بیماری در هر دو رقم شد. این نتایج اطلاعات جدیدی را درباره نقش بیوشیمیایی و مولکولی مسیرهای انتقال سیگنال فنیل پروپانوئید و اکتادکانوئید در مقاومت گندم در برابر گونه­های قارچ Fusarium ارائه می‌دهد.

کلیدواژه‌ها


عنوان مقاله [English]

Evaluating the role of phenylpropanoid and octadecanoid signal transduction pathways and some components of cell wall-associated defense in wheat cultivars- Fusarium species interaction*

نویسندگان [English]

  • N. Khaledi 1
  • P. Taheri 2
  • M. Falahati-Rastegar 3
1 . PhD Student, Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran
2 Associate Professor, Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran.
3 Professor, Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran.
چکیده [English]

Two species of Fusarium graminearum and F. culmorum are the main causal agents of wheat head blight worldwide. Currently, there is limited knowledge about the defense-signaling pathways and mechanisms involved in wheat cultivars basal resistance against Fusarium spp. Phenylalanine ammonia lyase (PAL) and lipoxygenase (LOX) enzymes, as main markers of phenylpropanoid and octadecanoid signal transduction pathways, may be involved in plant defense responses. In this research, the activity of two enzymes of PAL and LOX and expression of corresponding genes, also production of defense compounds such as phenolics and lignin were investigated in the leaves and spikes of susceptible (Falat) and partially resistant (Gaskozhen) wheat cultivars inoculated withtwo species of F. graminearum and F. culmorum. The results of this study showed that the activity of these two enzymes and production of phenolic compounds and lignin in leaves and spikes of Gaskozhen cultivar was higher than Falat. Expression analysis of the PAL and LOX genes revealed a direct correlation between enzymes activity and expression of the corresponding genes. In most of the studied times after inoculation, higher levels of enzymes activity, gene expression and phenolics and lignin production were observed in wheat-F. culmorum interaction. Application of PAL and LOX inhibitors increased disease development in both cultivars. These results provide novel information about the biochemical and molecular role of phenylpropanoid and octadecanoid signal transduction pathways in resistance of wheat against Fusarium spp.
 

کلیدواژه‌ها [English]

  • Fusarium culmorum
  • Fusarium graminearum
  • Lipoxygenase
  • Phenylalanine ammonia lyase
  • resistance
 
Adom, K.K. and Liu, R.H. 2002. Antioxidant activity of grains. Journal of Agricultural and Food Chemistry 50: 6182-6187.
Ameye, M., Audenaert, K., De Zutter, N., Steppe, K., Van Meulebroek, L., Vanhaecke, L., De Vleesschauwer, D., Haesaert, G. and Smagghe, G. 2015. Priming of wheat with the green leaf volatile z-3-hexenyl acetate enhances defense against Fusarium graminearum but boosts deoxynivalenol production. Plant Physiology 167: 1671-1684.
Bagal, U.R., Leebens-Mack, J. H., Lorenz, W.W. and Dean, J.F.D. 2012. The phenylalanine ammonia lyase (PAL) gene family shows a gymnosperm-specific lineage. BMC Genomics 13(Suppl 3), S1.
Balbi, V. and Devoto, A. 2008. Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytologist 177: 301-318.
Beccari, G., Covarelli, L. and Nicholson, P. 2011. Infection processes and soft wheat response to root rot and crown rot caused by Fusarium culmorum. Plant Pathology 60: 671-684.
Bellincampi, D., Cervone, F. and Lionetti, V. 2014. Plant cell wall dynamics and wall related susceptibility in plant-pathogen interactions. Frontiers in Plant Science 5: 228.
Bernusi, I., Ghanadha, M.R., Omidi, M., Samadi, B.Y. and Hosseinzadeh, A. 2002. Inheritance of resistance to fusarium within a spike of wheat. Pajouhesh and Sazandegi 63: 57-62. (In Farsi).
Bhaskara Reddy, M.V., Arul, J., Angers, P. and Couture, L. 1999. Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. Journal of Agricultural and Food Chemistry 47: 1208-1216.
Bhuiyan, N. H., Selvaraj, G., Wei, Y. and King, J. 2009. Role of lignification in plant defense. Plant Signaling & Behavior 4: 158-159.
Bollina, V. and Kushalappa, A.C. 2011. In vitro inhibition of trichothecene biosynthesis in Fusarium graminearum by resistance-related endogenous metabolites identified in barley. Mycology 2: 291-296.
Bollina, V., Kumaraswamy, G.K., Kushalappa, A.C., Choo, T.M., Dion, Y., Rioux, S., Faubert, D. and Hamzehzarghani, H. 2010. Mass spectrometry-based metabolomics application to identify quantitative resistance-related metabolites in barley against Fusarium head blight. Molecular Plant Pathology 11: 769-782.
Boudet, A.M. 2007. Evolution and current status of research in phenolic compounds. Phytochemistry 68: 2722-2735.
Boutigny, A.L., Atanasova-Pénichon, V., Benet, M., Barreau, C. and Richard-Forget, F. 2010. Natural phenolic acids from wheat bran inhibit Fusarium culmorum trichothecene biosynthesis in vitro by repressing Tri gene expression. European Journal of Plant Pathology 127: 275-286.
Boutigny, A.L., Barreau, C., Atanasova-Penichon, V., Verdal-Bonnin, M.N., Pinson-Gadais, L. and Richard-Forget, F. 2009. Ferulic acid, an efficient inhibitor of type B trichothecene biosynthesis and Tri gene expression in Fusarium liquid cultures. Mycological Research 113: 746-753.
Bradford, M.M. 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
Carver, T.L.W., Zeyen, R.J., Bushnell, W.R. and Robbins, M.P. 1994. Inhibition of phenylalanine ammonia lyase and cinnamyl alcohol dehydrogenase increases quantitative susceptibility of barley to powdery mildew (Erysiphe graminis D. C.). Physiological and Molecular Plant Pathology 44: 261-272.
Coram, T.E., Wang, M.N. and Chen, X.M. 2008. Transcriptome analysis of the wheat-Puccinia striiformis f. sp. tritici interaction. Molecular Plant Pathology 9: 157-169.
Cuzick, A., Maguire, K. and Hammond-Kosack, K.E. 2009. Lack of the plant signalling component SGT1b enhances disease resistance to Fusarium culmorum in Arabidopsis buds and flowers. New Phytologist 181: 901-912.
Dai, J., and Mumper, R.J. 2010. Plant Phenolics: Extraction, analysis and their antioxidant and anticancer properties. Molecules 15: 7313-7352.
De Ascensao, A.R.F.D.C. and Dubery, I. A. 2003. Soluble and wall-bound phenolics and phenolic polymers in Musa acuminata roots exposed to elicitors from Fusarium oxysporum f. sp. cubense. Phytochemistry 63: 679-686.
Desmond, O.J., Manners, J.M., Stephens, A.E., MacLean, D.J., Schenk, P.M., Gardiner, D.M., Munn, A.L. and Kazan, K. 2008. The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defence responses in wheat. Molecular Plant Pathology 9: 435-445.
Dickerson, D. P., Pascholati, S. F., Hagerman, A. E., Butler, L. G. and Nicholson, R. L. 1984. Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiological Plant Pathology 25: 111-123.
Ding, L., Xu, H., Yi, H., Yang, L., Kong, Z., Zhang, L., Xue, S., Jia, H. and Ma, Z. 2011. Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS ONE 6: e19008.
Doderer, A., Kokkelink, I., Van der Veen, S., Valk, B.E., Schram, A.W. and Douma, A.C. 1992. Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochimica et Biophysica Acta 1120: 97-104.
Ellinger, D., Sode, B., Falter, C. and Voigt, C. A. 2014. Resistance of callose synthase activity to free fatty acid inhibition as an indicator of Fusarium head blight resistance in wheat. Plant Signaling & Behavior 9 pii: e28982.
Farmer, E.E., Alméras, E. and Krishnamurthy, V. 2003. Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Current Opinion in Plant Biology 6: 372-378.
Forrer, H.R., Musa, T., Schwab, F., Jenny, E., Bucheli, T. D., Wettstein, F. E. and Vogelgsang, S. 2014. Fusarium head blight control and prevention of mycotoxin contamination in wheat with botanicals and tannic acid. Toxins 6: 830-849.
Fraser, C.M. and Chapple, C. 2011. The phenylpropanoid pathway in Arabidopsis. The Arabidopsis Book 9: e0152.
Geetha, N.P., Amruthesh, K.N., Sharathchandra, R.G. and Shetty, H.S. 2005. Resistance to downy mildew in pearl millet is associated with increased phenylalanine ammonia lyase activity. Functional Plant Biology 32: 267-275.
Gherbawy, Y.A., El-Tayeb, M.A., Maghraby, T.A., Shebany, Y.M. and El-Deeb, B.A. 2012. Response of antioxidant enzymes and some metabolic activities in wheat to Fusarium spp. infections. Acta Agronomica Hungarica 60: 319-333.
Gimenez-Ibanez, S. and Solano, R. 2013. Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Frontiers in Plant Science 4: 72.
Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205-227.
Golzar, H. 1989. Wheat head blight disease Investigation on the Causal agent, methods of infection and contamination via seed. Plant Disease 25: 17-25.
Gunnaiah, R. and Kushalappa, A.C. 2014. Metabolomics deciphers the host resistance mechanisms in wheat cultivar Sumai-3, against trichothecene producing and non-producing isolates of Fusarium graminearum. Plant Physiology and Biochemistry 83: 40-50.
Gunnaiah, R., Kushalappa, A.C., Duggavathi, R., Fox, S. and Somers, D.J. 2012. Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PLoS ONE 7(7): e40695.
Hamzehzarghani, H., Paranidharan, V., Abu-Nada, Y., Kushalappa, A.C., Dion, Y., Rioux, S., Comeau, A. and Marshall, W.D. 2008. Metabolite profiling coupled with statistical analyses for potential high-throughput screening of quantitative resistance to Fusarium head blight in wheat. Canadian Journal of Plant Pathology 30: 24-36.
Hukkanen, A.T., Kokko, H.I., Buchala, A.J., McDougall, G.J., Stewart, D., Karenlampi, S.O. and Karjalainen, R.O. 2007. Benzothiadiazole induces the accumulation of phenolics and improves resistance to powdery mildew in strawberries. Journal of Agricultural and Food Chemistry 55: 1862-1870.
Ji, X., Dong, B., Shiran, B., Talbot, M.J., Edlington, J. E., White, R. G., Gubler, F. and Dolferus, R. 2011. Control of abscisic acid catabolism and abscisic acid homoeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiology 156: 617-662.
Kang, Z., Buchenauer, H., Huang, L., Han, Q. and Zhang, H. 2008. Cytological and immunocytochemical studies on responses of wheat spikes of the resistant Chinese cv. Sumai 3 and the susceptible cv. Xiaoyan 22 to infection by Fusarium graminearum. European Journal of Plant Pathology 120: 383-396.
Kocha, A., Kumara, N., Weberb, L., Kellerc, H., Imania, J. and Kogela, K.H. 2013. Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase-encoding genes confers strong resistance to Fusarium species. Proceedings of the National Academy of Sciences USA 110: 19324-19329.
Kumaraswamy, K. G., Kushalappa, A. C., Choo, T. M., Dion, Y. and Rioux, S. 2011. Mass spectrometry based metabolomics to identify potential biomarkers for resistance in barley against fusarium head blight (Fusarium graminearum). Journal of Chemical Ecology 37: 846-856.
Li, G. and Yen, Y. 2008. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Science 48: 1888-1896.
Li, H. B., Cheng, K. W., Wong, C. C., Fan, K. W., Chen, F. and Jiang, Y. 2007. Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chemistry 102: 771-776.
Lionetti, V., Giancaspro, A., Fabri, E., Giove, S. L., Reem, N., Zabotina, O.A., Blanco, A., Gadaleta, A. and Bellincampi, D. 2015. Cell wall traits as potential resources to improve resistance of durum wheat against Fusarium graminearum. BMC Plant Biology 15: 6.
Lou, S.N., Lin, Y.S., Hsu, Y.S., Chiu, E.M. and Ho, C.T. 2014. Soluble and insoluble phenolic compounds and antioxidant activity of immature calamondin affected by solvents and heat treatment. Food Chemistry 161: 246-53.
Makandar, R., Nalam, V., Chaturvedi, R., Jeannotte, R., Sparks, A.A. and Shah, J. 2010. Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum. Molecular Plant-Microbe Interactions Journal 23: 861-870.
Makandar, R., Nalam, V.J., Lee, H., Trick, H.N., Dong, Y. and Shah, J. 2012. Salicylic acid regulates basal resistance to Fusarium head blight in wheat. Molecular Plant-Microbe Interactions Journal 25: 431-439.
Malihipoor, A., Okhovat, M. and Alizadeh, A. 2000. Analysis of development of wheat Fusarium head blight disease in the controlled environment using the epidemiologic models. The journal of science and research of plant diseases experts’ society of Iran 36: 1-2
Mandal, S. M., Chakraborty, D. and Dey, S. 2010. Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signaling & Behavior 5: 359-368.
Matern, U. and Kneusel, R.E. 1988. Phenolic compounds in plant disease resistance. Phytoparasitica 16: 153-170.
Menden, B., Kohlhoff, M. and Moerschbacher, B.M. 2007. Wheat cells accumulate a syringyl-rich lignin during the hypersensitive resistance response. Phytochemistry 68: 513-520.
Motallebi, P., Niknam, V., Ebrahimzadeh, H., Hashemi, M., Pisi, A., Prodi, A., Tonti, S. and Nipoti, P. 2015a. Methyl jasmonate strengthens wheat plants against root and crown rot pathogen Fusarium culmorum infection. Journal of Plant Growth Regulation 34: 624-636.
Motallebi, P., Niknam, V., Ebrahimzadeh, H., Tahmasebi Enferadi, S., and Hashemi, M., 2015b. The effect of methyl jasmonate on enzyme activities in wheat genotypes infected by the crown and root rot pathogen Fusarium culmorum. Acta Physiologiae Plantarum 37: 237.
Nafisi, M., Fimognari, L. and Sakuragi, Y. 2015. Interplays between the cell wall and phytohormones in interaction between plants and necrotrophic pathogens. Phytochemistry 112: 63-71.
Nalam, V.J., Alam, S., Keereetaweep, J., Venables, B., Burdan, D., Lee, H., Trick, H.N., Sarowar, S., Makandar, R. and Shah, J. 2015. Facilitation of Fusarium graminearum infection by 9-lipoxygenases in Arabidopsis and wheat. Molecular Plant-Microbe Interactions Journal 28: 1142-1152.
Nicholson, P., Simpson, D.R., Weston, G., Rezanoor, H. N., Lees, A. K., Parry, D.W. and Joyce, D. 1998. Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiology and Molecular Biology of Plants 53(1): 17-37.
Nicholson, R.L. and Hammerschmidt, R. 1992. Phenolic compounds and their role in disease resistance. Annual Review of Phytopathology 30: 369-389.
Parry, D.W., Jenkinson, J. and Mcleod, I. 1995. Fusarium ear blight (scab) in small grain cereals - a review. Plant pathology 44: 207-238.
Pasquali, M. and Migheli, Q. 2014. Genetic approaches to chemotype determination in type B-trichothecene producing Fusaria. International Journal of Food Microbiology 189: 164-182.
Pasquali, M., Giraud, F., Lasserre, J.P., Planchon, S., Hoffmann, L., Bohn, T. and Renaut, J. 2010. Toxin induction and protein extraction from Fusarium spp. cultures for proteomic studies. Journal of Visualized Experiments 16(36) pii: 1690.
Petti, C., Reiber, K., Ali, S. S., Berney, M. and Doohan, F. M. 2012. Auxin as a player in the biocontrol of Fusarium head blight disease of barley and its potential as a disease control agent. BMC Plant Biology 12: 224.
Pieterse, C.M.J., Leon-Reyes, A., Van der Ent, S. and Van Wees, S.C.M. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5: 308-316.
Pieterse, C.M.J., Van Der Does, D., Zamioudis, C., Leon-Reyes, A. and Van Wees, S.C. 2012. Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28: 489-521.
Pogorelko, G., Lionetti, V., Bellincampi, D. and Zabotina, O. 2013. Cell wall integrity: targeted post-synthetic modifications to reveal its role in plant growth and defense against pathogens. Plant Signaling and Behaviour 8: 1-8.
Purwar, S., Sundaram, S., Sinha, S., Gupta, A., Dobriyall, N. and Kumar, A. 2013. Expression and in silico characterization of Phenylalanine ammonium lyase against karnal bunt (Tilletia indica) in wheat (Triticum aestivum). Bioinformation 9: 1013-1018.
Robert-Seilaniantz, A., Grant, M. and Jones, J.D.G. 2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology 49: 317-343.
Ruiz-Lopez, N., Haslam, R.P., Usher, S., Napier, J.A. and Sayanova, O. 2015. An alternative pathway for the effective production of the omega-3 long-chain polyunsaturates EPA and ETA in transgenic oilseeds. Plant Biotechnology Journal 13: 1264-1275.
Sahu, R., Sharaff, M., Pradhan, M., Sethi, A., Bandyopadhyay, T., Mishra, V.K., Chand, R., Chowdhury, A.K., Joshi, A.K. and Pandey, S.P. 2016. Elucidation of defense-related signaling responses to spot blotch infection in bread wheat (Triticum aestivum L.). The Plant Journal 86: 35-49.
Scherm, B., Balmas, V., Spanu, F., Pani, G., Delogu, G., Pasquali, M. and Migheli, Q. 2013. Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Molecular Plant Pathology 14: 323-341.
Shin, S., Kim, K.H., Kang, C.S., Cho, K.M., Park, C.S., Okagaki, R., and Park, J.C. 2014. A simple method for the assessment of fusarium head blight resistance in Korean wheat seedlings inoculated with Fusarium graminearum. The Plant Pathology Journal 30: 25-32.
Siranidou, E., Kang, Z. and Buchenauer, H. 2002. Studies on symptom development, phenolic compounds and morphological defense responses in wheat cultivars differing in resistance to fusarium head blight. Journal of Phytopathology 150: 200-208.
Soltanloo, H., Ghadirzade Khorzoghi, E., Ramezanpour, S.S. and Kalateh Arabi, M. 2011. Genetic analysis of Fusarium head blight resistance in bread wheat. Australasian Plant Pathology 40: 453-460.
Sorahinobar, M., Niknam, V., Ebrahimzadeh, H., Soltanloo, H., Behmanesh, M. and Tahmasebi Enferadi, S. 2015. Central role of salicylic acid in resistance of wheat against Fusarium graminearum. Journal of Plant Growth Regulation 1-15.
Sorahinobar, M., Niknam, V., Ebrahimzadeh, H., Soltanloo, H., Moradi, B. and Bahram, M. 2016. Lack of association between Fusarium graminearum resistance in spike and crude extract tolerance in seedling of wheat. European Journal of Plant Pathology 144: 525-538.
Spoel, S.H. and Dong, X. 2008. Making sense of hormone crosstalk during plant immune responses. Cell Host & Microbe 3: 348–351.
Suzuki, S., Suzuki, Y., Yamamoto, N., Hattori, T., Sakamoto, M. and Umezawa, T. 2009. High-throughput determination of thioglycolic acid lignin from rice. Plant Biotechnology 26: 337-340.
Taheri, P. and Tarighi, S. 2010. Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-mediated priming of phenylpropanoid pathway. Journal of Plant Physiology 167: 201-208.
Taheri, P. and Tarighi, S. 2011. A survey on basal resistance and riboflavin-induced defense responnses of sugar beet against Rizoctonia solani. Journal of Plant Physiology 168: 1114-1122.
Underwood, W. 2012. The plant cell wall: a dynamic barrier against pathogen invasion. Frontiers in Plant Science 3: 85.
Vogt, T. 2010. Phenylpropanoid biosynthesis. Molecular Plant 3: 2-20.
Wang, Y., Chantreau, M., Sibout, R. and Hawkins, S. 2013. Plant cell wall lignification and monolignol metabolism. Frontiers in Plant Science 4: 220.
Yoshida, M., Kawada, N. and Nakajima, T. 2007. Effect of infection timing on Fusarium head blight and mycotoxin accumulation in open and closed-flowering barley. Phytopathology 97: 1054-1062.
Zhang, P., Zhou, M.P., Zhang, X., Huo, Y. and Ma, H.X. 2013. Change of defensive-related enzyme in wheat crown rot seedlings infected by Fusarium graminearum. Cereal Research Communications 41: 431-439.
Zhang, Z.Q., Xiang, J.J. and Zhou, L. M. 2015. Antioxidant activity of three components of wheat leaves: ferulic acid, flavonoids and ascorbic acid. Journal of Food Science and Technology 52: 7297-7304.
Zhou, K., Hao, J., Griffey, C., Chung, H., O'Keefe, S.F., Chen, J. and Hogan, S. 2007. Antioxidant properties of fusarium head blight-resistant and -susceptible soft red winter wheat grains grown in Virginia. Journal of Agricultural and Food Chemistry 55: 3729-3736.