Research in Plant Disease (식물병연구)

The Korean Society of Plant Pathology (한국식물병리학회)
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Disease Resistance-Based Management of Alternaria Black Spot in Cruciferous Crops

병 저항성 기반 십자화과 작물의 검은무늬병 관리

  • Young Hee Lee (Division of Horticultural Science, College of Agriculture and Life Sciences, Gyeongsang National University) ;
  • Su Min Kim (Division of Horticultural Science, College of Agriculture and Life Sciences, Gyeongsang National University) ;
  • Seoung Bin Lee (Division of Horticultural Science, College of Agriculture and Life Sciences, Gyeongsang National University) ;
  • Sang Hee Kim (Division of Applied Life Science (BK21 Four Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Byung-Wook Yun (Department of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University) ;
  • Jeum Kyu Hong (Division of Horticultural Science, College of Agriculture and Life Sciences, Gyeongsang National University)
  • 이영희 (경상국립대학교 농업생명과학대학 원예과학부) ;
  • 김수민 (경상국립대학교 농업생명과학대학 원예과학부) ;
  • 이승빈 (경상국립대학교 농업생명과학대학 원예과학부) ;
  • 김상희 (경상국립대학교 자연과학대학 응용생명과학부) ;
  • 윤병욱 (경북대학교 농업생명과학대학 응용생명과학부) ;
  • 홍점규 (경상국립대학교 농업생명과학대학 원예과학부)
  • Received : 2023.09.04
  • Accepted : 2023.10.25
  • Published : 2023.12.31
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Abstract

Alternaria black spots or blights in cruciferous crops have been devastating diseases worldwide and led to economic losses in broccoli, Chinese cabbage, kale, radish, rapeseed, etc. These diseases are caused by different Alternaria spp., including A. brassicae, A. brassicicola and A. raphani transmitted from infected seeds or insect vectors. Efforts to excavate disease resistance traits of cruciferous crops against Alternaria black spots or blights have been demonstrated. Genetic resource of disease resistance was investigated in the wild relatives of cruciferous crops, and different cultivars were screened under different inoculation conditions. Development of the disease-resistant lines against Alternaria black spots or blights was also tried via genetic transformation of the cruciferous crops using diverse plant defence-associated genes. Plant immunity activated by pre-treatment with chemicals, i. e. β-amino-n-butyric acid and melatonin, was suggested for reducing Alternaria black spots or blights in cruciferous crops. The disease resistance traits have also been evaluated in model plant Arabidopsis originating from different habitats. Various plant immunity-related mutants showing different disease responses from wild-type Arabidopsis provided valuable information for managing Alternaria black spots or blights in cruciferous crops. In particular, redox regulation and antioxidant responses altered in the Alternaria-infected mutants were discussed in this review.

검은무늬병은 세계적으로 재배되는 십자화과 작물을 황폐화시키고 있으며, 브로콜리, 배추, 케일, 무, 유채 등의 생산에 경제적인 손실을 가져왔다. 십자화과 작물의 검은무늬병은 A. brassicae, A. brassicicola, A. raphani 등을 포함하는 다수의 Alternaria 종에 의하여 발생하며 이러한 병원균들은 감염된 종자나 매개충에 의하여 전반된다. 본 총설에서는 검은무늬병에 대한 십자화과 작물의 병 저항성 형질을 발굴하기 위한 그 동안의 노력을 보여주었다. 병 저항성을 위한 유전 자원이 십자화과 작물의 근연 야생종으로부터 조사되었으며, 십자화과 작물의 상이한 품종들이 다른 접종 조건에서 선별되었다. 검은무늬병 저항성 작물의 개발을 위하여 다양한 식물 방어 관련 유전자들을 이용한 십자화과 작물의 형질 전환이 이루어지기도 하였다. β-Amino-n-butyric acid나 멜라토닌과 같은 화학 물질을 전처리하여 활성화된 식물 면역이 십자화과 작물의 검은무늬병을 줄이기 위하여 제안되었다. 검은무늬병 저항성 형질은 다른 서식지에서 유래한 모델 식물 Arabidopsis 생태형들에서도 평가되었다. 야생형 Arabidopsis와는 상이한 병 저항성을 보이는 식물 면역 관련 돌연변이체들은 십자화과 작물에서 검은무늬병을 관리하는 데에 가치있는 정보를 제공하였다. 특히 이러한 돌연변이체에서 변동된 산화-환원 조절과 항산화 반응에 대하여 본 총설에서 논하였다.

Keywords

Acknowledgement

This work was financially supported by National Research Foundation (NRF) of Korea, Ministry of Education, Science and Technology (MEST) of Korea government (grant no. NRF2020R1A2C1101613), Republic of Korea.

References

  1. Alam, M. M., Nahar, K., Hasanuzzaman, M. and Fujita, M. 2014. Alleviation of osmotic stress in Brassica napus, B. campestris, and B. juncea by ascorbic acid application. Biol. Plant. 58: 697-708. https://doi.org/10.1007/s10535-014-0447-0
  2. Ali, S., Gill, R. A., Ulhassan, Z., Zhang, N., Hussain, S., Zhang, K. et al. 2023. Exogenously applied melatonin enhanced the tolerance of Brassica napus against cobalt toxicity by modulating antioxidant defense, osmotic adjustment, and expression of stress response genes. Ecotoxic. Environ. Saf. 252: 114624.
  3. Ali, S., Mir, Z. A., Tyagi, A., Mehari, H., Meena, R. P., Bhat, J. A. et al. 2017. Overexpression of NPR1 in Brassica juncea confers broad spectrum resistance to fungal pathogens. Front. Plant Sci. 8: 1693.
  4. Al-Lami, H. F. D., You, M. P., Banga, S. S. and Barbetti, M. J. 2023. Novel resistances provide new avenues to manage Alternaria leaf spot (Alternaria brassicae) in canola (Brassicae napus), mustard (B. juncea), and other Brassicaceae crops. Plant Dis. 107: 372-381. https://doi.org/10.1094/PDIS-05-22-1153-RE
  5. Al-Lami, H. F. D., You, M. P. and Barbetti, M. J. 2020. Temperature drives contrasting Alternaria leaf spot epidemic development in canola and mustard rape from Alternaria japonica and A. brassicae. Plant Dis. 104: 1668-1674. https://doi.org/10.1094/PDIS-10-19-2251-RE
  6. Arratia-Castro, A. A., Fernandez-Herrera, E., Gomez-Espinoza, M. G., Herrera-Flores, T. S., Moreno-Contreras, M. G., Licea-de Anda, E. M. et al. 2022. Alternaria alternata, Fusarium oxysporum and Fusarium verticillioides identified as causal agents of broccoli head rot in Mexico. Rev. Chapingo Ser. Hortic. 28: 175-188.
  7. Balmer, A., Glauser, G., Mauch-Mani, B. and Bacclli, I. 2019. Accumulation patterns of endogenous β-aminobutyric acid during plant development and defence in Arabidopsis thaliana. Plant Biol. 21: 318-325. https://doi.org/10.1111/plb.12940
  8. Blagojevic, J. D., Vukojevic, J. B. and Ivanovic, Z. S. 2020. Occurrence and characterization of Alternaria species associated with leaf spot disease in rapeseed in Serbia. Plant Pathol. 69: 883-900. https://doi.org/10.1111/ppa.13168
  9. Botanga, C. J., Bethke, G., Chen, Z., Gallie, D. R., Fiehn, O. and Glazebrook, J. 2012. Metabolite profiling of Arabidopsis inoculated with Alternaria brassicicola reveals that ascorbate reduces disease severity. Mol. Plant-Microbe Interact. 25: 1628-1638. https://doi.org/10.1094/MPMI-07-12-0179-R
  10. Brazauskiene, I. and Petraitiene, E. 2002. Dark leaf and pod spot (Alternaria brassicae) on oilseeds (Brassica napus) in Lithuania. Plant Prot. Sci. 38: 384-387. https://doi.org/10.17221/10498-PPS
  11. Cabral, C. S., Barboza, E. A., Lopes, L. H. R., Rossato, M., Borges, R. C. F. and Reis, A. 2020. Characterization of Alternaria isolates causing leaf spots in radish in Brazil. Summa Phytopathol. 46: 340-341. https://doi.org/10.1590/0100-5405/233817
  12. Caesar, A. J. and Lartey, R. T. 2009. First report of a leaf spot caused by Alternaria brassicae on the invasive weed Lepidium draba in North America. Plant Dis. 93: 846.
  13. Chavan, A., Bhargava, S. and Kamble, A. 2013. Temporal modulation of oxidant and antioxidative responses in Brassica carinata during β-aminobutyric acid-induced resistance against Alternaria brassicae. Physiol. Mol. Plant Pathol. 83: 35-39. https://doi.org/10.1016/j.pmpp.2013.03.002
  14. Chavan, V. and Kamble, A. 2013. β-Aminobutyric acid primed expression of WRKY and defence genes in Brassica carinata against Alternaria blight. J. Phytopathol. 161: 859-865. https://doi.org/10.1111/jph.12132
  15. Chavan, V. and Kamble, A. 2014. Induction of total phenolics and defence-related enzymes during β-aminobutyric acid-induced resistance in Brassica carinata against Alternaria blight. Arch. Phytopathol. Plant Pathol. 47: 2200-2212. https://doi.org/10.1080/03235408.2013.870697
  16. Chen, X., Laborda, P. and Liu, F. 2020. Exogenous melatonin enhances rice plant resistance against Xanthomonas oryzae pv. oryzae. Plant Dis. 104: 1701-1708. https://doi.org/10.1094/PDIS-11-19-2361-RE
  17. Cobb, A. C. and Dillard, H. R. 1998. Thlaspi arvense, a new host for Alternaria brassicicola. Plant Dis. 82: 960.
  18. Datta, R., Mandal, K., Boro, P., Sultana, A. and Chattopadhyay, S. 2022. Glutathione imparts stress tolerance against Alternaria brassicicola infection via miRNA mediated gene regulation. Plant Signal. Behav. 17: 2047352.
  19. de Freitas, M. B. and Stadnik, M. J. 2015. Ulvan-induced resistance in Arabidopsis thaliana against Alternaria brassicicola requires reactive oxygen species derived from NADPH oxidase. Physiol. Mol. Plant Pathol. 90: 49-56. https://doi.org/10.1016/j.pmpp.2015.03.002
  20. Deng, J. X., Li, M. J., Paul, N. C., Oo, M. M., Lee, H. B., Oh, S.-K. et al. 2018. Alternaria brassicifolii sp. nov. isolated from Brassica rapa subsp. pekinensis in Korea. Mycobiology 46: 172-176. https://doi.org/10.1080/12298093.2018.1468054
  21. Dethoup, T., Songkumarn, P., Rueangrit, S., Suesa-ard, S. and Kaewkrajay, C. 2018. Fungicidal activity of Thai medicinal plant extracts against Alternaria brassicicola causing black spot of Chinese kale. Eur. J. Plant Pathol. 152: 157-167. https://doi.org/10.1007/s10658-018-1460-5
  22. Dillard, H. R., Cobb, A. C. and Lamboy, J. S. 1998. Transmission of Alternaria brassicicola to cabbage by flea beetles (Phyllotreta cruciferae). Plant Dis. 82: 153-157. https://doi.org/10.1094/PDIS.1998.82.2.153
  23. Doughty, K. J., Porter, A. J. R., Morton, A. M., Kiddle, G., Bock, C. H. and Wallsgrove, R. 1991. Variation in the glucosinolate content of oilseed rape (Brassica napus L.) leaves. II. Response to infection by Alternaria brassicae (Berk.) Sacc. Ann. Appl. Biol. 118: 469-477. https://doi.org/10.1111/j.1744-7348.1991.tb05648.x
  24. Doullah, M. A. U., Meah, M. B. and Okazaki, K. 2006. Development of an effective screening method for partial resistance to Alternaria brassicicola (dark leaf spot) in Brassica rapa. Eur. J. Plant Pathol. 116: 33-43. https://doi.org/10.1007/s10658-006-9035-2
  25. Farahani, A. S. and Taghavi, S. M. 2017. Induction of resistance in pepper against Xanthomonas euvesicatoria by β-aminobutyric acid. Australas. Plant Dis. Notes 12: 1.
  26. Hassan, N., Nakasuji, S., Elsharkawy, M. M., Nazmin, H. A., Kubota, M., Ketta, H. et al. 2017. Biocontrol potential of an endophytic Streptomyces sp. strain MBCN152-1 against Alternaria brassicicola on cabbage plug seedlings. Microbes Environ. 32: 133-141. https://doi.org/10.1264/jsme2.ME17014
  27. Ji, H., Kyndt, T., He, W., Vanholme, B. and Gheysen, G. 2015. β-Aminobutyric acid-induced resistance against root-knot nematodes in rice is based on increased basal defense. Mol. Plant-Microbe Interact. 28: 519-533. https://doi.org/10.1094/MPMI-09-14-0260-R
  28. Jia, C., Yu, X., Zhang, M., Liu, Z., Zou, P., Ma, J. et al. 2020. Application of melatonin-enhanced tolerance to high-temperature stress in cherry radish (Raphanus sativus L. var. radculus pers). J. Plant Growth Regul. 39: 631-640. https://doi.org/10.1007/s00344-019-10006-1
  29. Jung, H.-I., Lee, T.-G., Lee, J., Chae, M.-J., Lee, E.-J., Kim, M.-S. et al. 2021. Foliar-applied glutathione mitigates cadmium-induced oxidative stress by modulating antioxidant-scavenging, redoxregulating, and hormone-balancing systems in Brassica napus. Front. Plant Sci. 12: 700413.
  30. Kagan, I. A. and Hammerschmidt, R. 2002. Arabidopsis ecotype variability in camalexin production and reaction to infection by Alternaria brassicicola. J. Chem. Ecol. 28: 2121-2140. https://doi.org/10.1023/A:1021020512846
  31. Kaman-Toth, E., Danko, T., Gullner, G., Bozso, Z., Palkovics, L. and Pogany, M. 2019. Contribution of cell wall peroxidase- and NADPH oxidase-derived reactive oxygen species to Alternaria brassicicola-induced oxidative burst in Arabidopsis. Mol. Plant Pathol. 20: 485-499. https://doi.org/10.1111/mpp.12769
  32. Kamble, A. and Bhargava, S. 2007. β-Aminobutyric acid-induced resistance in Brassica juncea against the necrotrophic pathogen Alternaria brassicae. J. Phytopathol. 155: 152-158. https://doi.org/10.1111/j.1439-0434.2007.01209.x
  33. Kamble, A., Koopmann, B. and von Tiedemann, A. 2013. Induced resistance to Verticillium longisporum in Brassica napus by β-aminobutyric acid. Plant Pathol. 62: 552-561. https://doi.org/10.1111/j.1365-3059.2012.02669.x
  34. Kamble, S., Mukherjee, P. K. and Eapen, S. 2016. Expression of an endochitinase gene from Trichoderma virens confers enhanced tolerance to Alternaria blight in transgenic Brassica juncea (L.) czern and coss lines. Physiol. Mol. Biol. Plants 22: 69-76. https://doi.org/10.1007/s12298-016-0340-8
  35. Keinath, A. P., Toporek, S. M., DuBose, V. B., Zardus, S. H. and Ballew, J. B. 2021. First report of Alternaria japonica, a causal agent of black spot, on kale in South Carolina, U.S.A. Plant Dis. 105: 2016.
  36. Kim, Y. C., Kim, Y. H., Lee, Y. H., Lee, S. W., Chae, Y.-S., Kang, H.-K. et al. 2013. β-Amino-n-butyric acid regulates seedling growth and disease resistance of kimchi cabbage. Plant Pathol. J. 29: 305-316. https://doi.org/10.5423/PPJ.OA.12.2012.0191
  37. Komhorm, A., Thongmee, S., Thammakun, T., Oiuphisittraiwat, T. and Jantason, A. 2021. In vivo testing of antagonistic fungi against Alternaria brassicicola causing Chinese kale black spot disease. J. Plant Dis. Prot. 128: 183-189. https://doi.org/10.1007/s41348-020-00382-2
  38. Kreis, R. A., Dillard, H. R. and Smart, C. D. 2016. Population diversity and sensitivity to azoxystrobin of Alternaria brassicicola in New York State. Plant Dis. 100: 2422-2426. https://doi.org/10.1094/PDIS-03-16-0414-RE
  39. Kwon, S. J., Jin, H. C., Lee, S., Nam, M. H., Chung, J. H., Kwon, S. I. et al. 2009. GDSL lipase-like 1 regulates systemic resistance associated with ethylene signaling in Arabidopsis. Plant J. 58: 235-245. https://doi.org/10.1111/j.1365-313X.2008.03772.x
  40. Latif, M., Akram, N. A. and Ashraf, M. 2016. Regulation of some biochemical attributes in drought-stressed cauliflower (Brassica oleracea L.) by seed pre-treatment with ascorbic acid. J. Hortic. Sci. Biotechnol. 91: 129-137. https://doi.org/10.1080/14620316.2015.1117226
  41. Lee, J. H., Jang, K. S., Choi, Y. H., Kim, H. and Choi, G. J. 2017. Development of an effective method for testing resistance to black spot of radish caused by Alternaria brassicicola. Hortic. Sci. Technol. 35: 210-219. (In Korean) https://doi.org/10.12972/kjhst.20170024
  42. Lee, J., Lee, H., Wi, S., Yu, I., Yeo, K.-H., An, S. et al. 2021. Enhancement of growth and antioxidant enzyme activities on kimchi cabbage by melatonin foliar application under high temperature and drought stress conditions. Hortic. Sci. Technol. 39: 583-592. (In Korean) https://doi.org/10.7235/HORT.20210052
  43. Lee, S. M., Choi, Y. H., Lee, J. J., Kim, H. and Choi, G. J. 2022. Development of an efficient screening method for Chinese cabbage cultivars resistant to Alternaria brassicicola and determination of their resistance characteristics. Hortic. Sci. Technol. 40: 94-108. (In Korean) https://doi.org/10.7235/HORT.20220010
  44. Lee, Y. H. and Hong, J. K. 2015. Differential defence responses of susceptible and resistant kimchi cabbage cultivars to anthracnose, black spot and black rot diseases. Plant Pathol. 64: 406-415. https://doi.org/10.1111/ppa.12262
  45. Lee, Y. H., Kim, Y. J., Moon, J. Y., Kim, H. J., Park, J. M., Hwang, I. S. et al. 2019. Response of two Arabidopsis ecotypes Columbia-0 and Dijon-G to necrotrophic and biotrophic pathogens. Biol. Plant. 63: 654-661. https://doi.org/10.32615/bp.2019.071
  46. Lei, Y., He, H., Raza, A., Liu, Z., Xiaoyu, D., Guijuan, W. et al. 2022. Exogenous melatonin confers cold tolerance in rapeseed (Brassica napus L.) seedlings by improving antioxidants and genes expression. Plant Signal. Behav. 17: 2129289.
  47. Li, C., He, Q., Zhang, F., Yu, J., Li, C., Zhao, T. et al. 2019. Melatonin enhances cotton immunity to Verticillium wilt via manipulating lignin and gossypol biosynthesis. Plant J. 100: 784-800. https://doi.org/10.1111/tpj.14477
  48. Li, J., Huang, T., Xia, M., Lu, J., Xu, X., Liu, H. et al. 2023. Exogenous melatonin mediates radish (Raphanus sativus) and Alternaria brassicae interaction in a dose-dependent manner. Front. Plant Sci. 14: 1126669.
  49. Li, R., Sheng, J. and Shen, L. 2020. Nitric oxide plays an important role in β-aminobutyric acid-induced resistance to Botrytis cinerea in tomato plants. Plant Pathol. J. 36: 121-132. https://doi.org/10.5423/PPJ.OA.11.2019.0274
  50. Lin, T.-C., Fan, M.-C., Wang, S.-Y. and Huang, J.-W. 2011. Identification of the Solanum nigrum extract component involved in controlling cabbage black leaf spot disease. J. Agric. Food Chem. 59: 1667-1672. https://doi.org/10.1021/jf103698b
  51. Liu, C., Chen, L., Zhao, R., Li, R., Zhang, S., Yu, W. et al. 2019. Melatonin induces disease resistance to Botrytis cinerea in tomato fruit by activating jasmonic acid signaling pathway. J. Agric. Food Chem. 67: 6116-6124. https://doi.org/10.1021/acs.jafc.9b00058
  52. Macagnan, D., Chaves, Z. M. and Cafe-Filho, A. C. 2010. First report of Alternaria brassicicola on Crambe abyssinica in Goias state, Brazil. Summa Phytopathol. 36: 260.
  53. Mandal, M. K., Suren, H., Ward, B., Boroujerdi, A. and Kousik, C. 2018. Differential roles of melatonin in plant-host resistance and pathogen suppression in cucurbits. J. Pineal Res. 65: e12505.
  54. Mandal, S., Rajarammohan, S. and Kaur, J. 2019. ROS accumulation and associated cell death mediates susceptibility to Alternaria brassicae in Arabidopsis accessions. Physiol. Mol. Plant Pathol. 107: 51-59. https://doi.org/10.1016/j.pmpp.2019.06.001
  55. Mazumder, M., Das, S., Saha, U., Chatterjee, M., Bannerjee, K. and Basu, D. 2013. Salicylic acid-mediated establishment of the compatibility between Alternaria brassicicola and Brassica juncea is mitigated by abscisic acid in Sinapis alba. Plant Physiol. Biochem. 70: 43-51. https://doi.org/10.1016/j.plaphy.2013.04.025
  56. Michereff, S. J., Noronha, M. A., Filha, M. S. X., Camara, M. P. S. and Reis, A. 2012. Survey and prevalence of species causing Alternaria leaf spots on brassica species in Pernambuco. Hortic. Bras. 30: 345-348. https://doi.org/10.1590/S0102-05362012000200027
  57. Mondal, K. K., Bhattacharya, R. C., Koundal, K. R. and Chatterjee, S. C. 2007. Transgenic Indian mustard (Brassica juncea) expressing tomato glucanase leads to arrested growth of Alternaria brassicae. Plant Cell Rep. 26: 247-252. https://doi.org/10.1007/s00299-006-0241-3
  58. Mondal, K. K., Chatterjee, S. C., Viswakarma, N., Bhattacharya, R. C. and Grover, A. 2003. Chitinase-mediated inhibitory activity of Brassica transgenic on growth of Alternaria brassicae. Curr. Microbiol. 47: 171-173. https://doi.org/10.1007/s00284-002-3980-6
  59. Mora, A. A. and Earle, E. D. 2001. Resistance to Alternaria brassicicola in transgenic broccoli expressing a Trichoderma harzianum endochitinase gene. Mol. Breed. 8: 1-9. https://doi.org/10.1023/A:1011913100783
  60. Mukherjee, A. K., Lev, S., Gepstein, S. and Horwitz, B. A. 2009. A compatible interaction of Alternaria brassicicola with Arabidopsis thaliana ecotype DiG: evidence for a specific transcriptional signature. BMC Plant Biol. 9: 31.
  61. Muto, M., Mulabagal, V., Huang, H.-C., Takahashi, H., Tsay, H.-S. and Huang, J.-W. 2006. Toxicity of black nightshade (Solanum nigrum) extracts on Alternaria brassicicola, causal agent of black leaf spot of Chinese cabbage (Brassica pekinensis). J. Phytopathol. 154: 45-50. https://doi.org/10.1111/j.1439-0434.2005.01059.x
  62. Nakamura, S., Suzui, N., Nakasaka, T., Komatsu, F., Ishioka, N. S., ItoTanabata, S. et al. 2013. Application of glutathione to roots selectively inhibits cadmium transport from roots to shoots in oilseed rape. J. Exp. Bot. 64: 1073-1081. https://doi.org/10.1093/jxb/ers388
  63. Nieto-Lopez, E. H., Cerritos-Garcia, D. G., Bach, R. A. K., Petkar, A., Smart, C. D., Hoepting, C. et al. 2023. Species identification and fungicide sensitivity of fungi causing Alternaria leaf blight and head rot in cole crops in the eastern United States. Plant Dis. 107: 1310-1315.
  64. Nira, S. T., Hossain, M. F., Mahmud, N. U., Hassan, O., Islam, T. and Akanda, A. M. 2022. Alternaria leaf spot of broccoli caused by Alternaria alternata in Bangladesh. Plant Prot. Sci. 58: 49-56. https://doi.org/10.17221/44/2020-PPS
  65. Oh, I. S., Park, A. R., Bae, M. S., Kwon, S. J., Kim, Y. S., Lee, J. E. et al. 2005. Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 17: 2832-2847. https://doi.org/10.1105/tpc.105.034819
  66. Pajot, E. and Silue, D. 2005. Evidence that DL-3-aminobutyric acid and acibenzolar-S-methyl induce resistance against bacterial head rot disease of broccoli. Pest Manag. Sci. 61: 1110-1114. https://doi.org/10.1002/ps.1103
  67. Parisy, V., Poinssot, B., Owsianowski, L., Buchala, A., Glazebrook, J. and Mauch, F. 2006. Identification of PAD2 as γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J. 49: 159-172. https://doi.org/10.1111/j.1365-313X.2006.02938.x
  68. Park, H.-S., Kazerooni, E. A., Kang, S.-M., Al-Sadi, A. M. and Lee, I.-J. 2021. Melatonin enhances the tolerance and recovery mechanisms in Brassica juncea (L.) Czern. under saline conditions. Front. Plant Sci. 12: 593717.
  69. Penninckx, I. A. M. A., Thomma, B. P. H. J., Buchala, A., Metraux, J.-P. and Broekaert, W. F. 1998. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103-2113. https://doi.org/10.1105/tpc.10.12.2103
  70. Pogany, M., von Rad, U., Grun, S., Dongo, A., Pintye, A., Simoneau, P. et al. 2009. Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiol. 151: 1459-1475. https://doi.org/10.1104/pp.109.141994
  71. Poursafar, A., Ghosta, Y. and Azizi, R. 2020. Alternaria telliensis, a new causal agent of cabbage leaf spot in Iran. Mycol. Iran. 7: 231-239.
  72. Raghavendra, B. T. and Singh, D. 2017. Effect of β-amino butyric acid induction of resistance against Xanthomonas campestris pv. campestris in cabbage. Indian Phytopathol. 70: 384-387. https://doi.org/10.24838/ip.2017.v70.i3.74247
  73. Rahimloo, T. and Ghosta, Y. 2015. The occurrence of Alternaria species on cabbage in Iran. Zemdirbyste-Agriculture 102: 343-350. https://doi.org/10.13080/z-a.2015.102.044
  74. Rajarammohan, S., Kumar, A., Gupta, V., Pental, D., Pradhan, A. K. and Kaur, J. 2017. Genetic architecture of resistance to Alternaria brassicae in Arabidopsis thaliana: QTL mapping reveals two major resistance-conferring loci. Front. Plant Sci. 8: 260.
  75. Rajarammohan, S., Pradhan, A. K., Pental, D. and Kaur, J. 2018. Genome-wide association mapping in Arabidopsis identifies novel genes underlying quantitative disease resistance to Alternaria brassicae. Mol. Plant Pathol. 19: 1719-1732. https://doi.org/10.1111/mpp.12654
  76. Reis, A. and Boiteux, L. S. 2010. Alternaria species infecting Brassicaceae in the Brazilian neotropics: geographical distribution, host range and specificity. J. Plant Pathol. 92: 661-668.
  77. Roylawar, P. and Kamble, A. 2017. β-amino butyric acid mediated changes in cellular redox homeostasis confers tomato resistance to early blight. Australas. Plant Pathol. 16: 239-249. https://doi.org/10.1007/s13313-017-0484-1
  78. Saha, U., Mazumder, M., Mukherjee, A., Parveen, S., Mondal, B., Maji, S. R. et al. 2016. A critical analysis of phosphatidic acid mediated resistance response in Sinapis alba against Alternaria brassicicola. Physiol. Mol. Plant Pathol. 94: 90-99. https://doi.org/10.1016/j.pmpp.2016.05.003
  79. Sami, A., Shah, F. A., Abdullah, M., Zhou, X., Yan, Y., Zhu, Z. et al. 2020. Melatonin mitigates cadmium and aluminium toxicity through modulation of antioxidant potential in Brassica napus L. Plant Biol. 22: 679-690. https://doi.org/10.1111/plb.13093
  80. Shekhar, S., Panwar, R., Prasad, S. C., Kumar, D. and Rustagi, A. 2023. Overexpression of flowering locus D (FLD) in Indian mustard (Brassica juncea) enhances to tolerance to Alternaria brassicae and Sclerotinia sclerotiorum. Plant Cell Rep. 42: 1233-1250. https://doi.org/10.1007/s00299-023-03021-w
  81. Shi, X., Zeng, K., Wang, X., Liang, Z. and Wu, X. 2021. Characterization of Alternaria species causing leaf spot on Chinese cabbage in Shanxi province of China. J. Plant Pathol. 103: 283-293. https://doi.org/10.1007/s42161-020-00740-x
  82. Shivanna, K. R. and Sawhney, V. K. 1993. Pollen selection for Alternaria resistance in oilseed brassicas: responses of pollen grains and leaves to a toxin of A. brassicae. Theor. Appl. Genet. 86: 339-344. https://doi.org/10.1007/BF00222099
  83. Siemens, J. 2002. Interspecific hybridisation between wild relatives and Brassica napus to introduce new resistance traits into the oilseed rape gene pool. Czech J. Genet. Plant Breed. 38: 155-157. https://doi.org/10.17221/6258-CJGPB
  84. Sigareva, M. A. and Earle, E. D. 1999. Camalexin induction in intertribal somatic hybrids between Camelina sativa and rapidcycling Brassica oleracea. Theor. Appl. Genet. 98: 164-170. https://doi.org/10.1007/s001220051053
  85. Silue, D., Pajot, E. and Cohen, Y. 2002. Induction of resistance to downy mildew (Peronospora parasitica) in cauliflower by DL-β-amino-n-butanoic acid (BABA). Plant Pathol. 51: 97-102. https://doi.org/10.1046/j.1365-3059.2002.00649.x
  86. Tang, M., Xu, L., Wang, Y., Dong, J., Zhang, X., Wang, K. et al. 2021. Melatonin-induced DNA demethylation of metal transporters and antioxidant genes alleviates lead stress in radish plants. Hortic. Res. 8: 124.
  87. Thevenet, D., Pastor, V., Baccelli, I., Balmer, A., Vallet, A., Neier, R. et al. 2017. The priming molecule β-aminobutyric acid is naturally present in plants and is induced by stress. New Phytol. 213: 552-559. https://doi.org/10.1111/nph.14298
  88. Thomma, B. P. H. J., Eggermont, K., Broekaert, W. F. and Cammue, B. P. A. 2000. Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol. Biochem. 38: 421-427. https://doi.org/10.1016/S0981-9428(00)00756-7
  89. Thomma, B. P. H. J., Eggermont, K., Penninckx, I. A. M. A., MauchMani, B., Vogelsang, R., Cammue, B. P. A. et al. 1998. Separate jasmonate-dependent and salicylate-dependent defenseresponse pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. U. S. A. 95: 15107-15111. https://doi.org/10.1073/pnas.95.25.15107
  90. Thomma, B. P. H. J., Nelissen, I., Eggermont, K. and Broekaert, W. F. 1999. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J. 19: 163-171. https://doi.org/10.1046/j.1365-313X.1999.00513.x
  91. Tierens, K. F. M.-J., Thomma, B. P. H. J., Bari, R. P., Garmier, M., Eggermont, K., Brouwer, M. et al. 2002. Esa1, an Arabidopsis mutant with enhanced susceptibility to a range of necrotrophic fungal pathogens, shows a distorted induction of defense responses by reactive oxygen generating compounds. Plant J. 29: 131-140. https://doi.org/10.1046/j.1365-313x.2002.01199.x
  92. Ulhassan, Z., Huang, Q., Gill, R. A., Ali, S., Mwamba, T. M., Ali, B. et al. 2019. Protective mechanisms of melatonin against selenium toxicity in Brassica napus: insights into physiological traits, thiol biosynthesis and antioxidant machinery. BMC Plant Biol. 19: 507.
  93. van Wees, S. C. M., Chang, H.-S., Zhu, T. and Glazebrook, J. 2003. Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol. 132: 606-617. https://doi.org/10.1104/pp.103.022186
  94. Verma, S. S., Yajima, W. R., Rahman, M. H., Shah, S., Liu, J.-J., Ekramoddoullah, A. K. M. et al. 2012. A cysteine-rich antimicrobial peptide from Pinus monticola (PmAMP1) confers resistance to multiple fungal pathogens in canola (Brassica napus). Plant Mol. Biol. 79: 61-74. https://doi.org/10.1007/s11103-012-9895-0
  95. Wang, B., Lou, T., Wei, L., Chen, W., Huang, L., Ding, L. et al. 2021. Biochemical and molecular characterization of Alternaria alternata isolates highly resistant to procymidone from broccoli and cabbage. Phytopathol. Res. 3: 15.
  96. Wang, K., Wu, D., Bo, Z., Chen, S., Wang, Z., Zheng, Y. et al. 2019. Regulation of redox status contributes to priming defense against Botrytis cinerea in grape berries treated with β-aminobutyric acid. Sci. Hortic. 244: 352-364. https://doi.org/10.1016/j.scienta.2018.09.074
  97. Wang, M., Li, Y., Li, C., Xu, H., Sun, T. and Ge, Y. 2023. Melatonin induces resistance against Penicillium expansum in apple fruit through enhancing phenylpropanoid metabolism. Physiol. Mol. Plant Pathol. 127: 102082.
  98. Westman, A. L., Kresovich S. and Dickson, M. H. 1999. Regional variation in Brassica nigra and other weedy crucifers for disease reaction to Alternaria brassicicola and Xanthomonas campestris pv. campestris. Euphytica 106: 253-259. https://doi.org/10.1023/A:1003544025146
  99. Wu, J.-J., Chou, H.-P., Huang, J. W. and Deng, W.-L. 2021. Genomic and biochemical characterization of antifungal compounds produced by Bacillus subtilis PMB102 against Alternaria brassicicola. Microbiol. Res. 251: 126815.
  100. Yang, Y. N., Kim, Y., Kim, H., Kim, S. J., Cho, K.-M., Kim, Y. et al. 2021. The transcription factor ORA59 exhibits dual DNA binding specificity that differentially regulates ethylene- and jasmonic acid-induced genes in plant immunity. Plant Physiol. 187: 2763-2784. https://doi.org/10.1093/plphys/kiab437
  101. Yin, L., Wang, P., Li, M., Ke, X., Li, C., Liang, D. et al. 2013. Exogenous melatonin improves Malus resistance to Marssonina apple blotch. J. Pineal Res. 54: 426-434. https://doi.org/10.1111/jpi.12038
  102. You, M. P., Simoneau, P., Dongo, A., Barbetti, M. J., Li, H. and Sivasithamparam, K. 2005. First report of an Alternaria leaf spot caused by Alternaria brassicae on Crambe abyssinicia in Australia. Plant Dis. 89: 430.
  103. Yu, S. H., Yun, H. K., Park, C. H. and Lee, H. B. 1991. Three species of Alternaria associated with Alternaria leaf spot of radish in Korea. Korean J. Plant Pathol. 7: 188-191. (In Korean)
  104. Zhang, S., Zheng, X., Reiter, R. J., Feng, S., Wang, Y., Liu, S. et al. 2017. Melatonin attenuates potato late blight by disrupting cell growth, stress tolerance, fungicide susceptibility and homeostasis of gene expression in Phytophthora infestans. Front. Plant Sci. 8: 1993.