Enhanced Tolerance of Chinese Cabbage Seedlings Mediated by Bacillus aryabhattai H26-2 and B. siamensis H30-3 against High Temperature Stress and Fungal Infections

  • Lee, Young Hee (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Jang, Su Jeong (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Han, Joon-Hee (Division of Bioresource Sciences, Kangwon National University) ;
  • Bae, Jin Su (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Shin, Hyunsuk (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech)) ;
  • Park, Hee Jin (Institute of Glocal Disease Control, Konkuk University) ;
  • Sang, Mee Kyung (National Institute of Agricultural Science, Rural Development Administration) ;
  • Han, Song Hee (Hyunnong Co., Ltd) ;
  • Kim, Kyoung Su (Division of Bioresource Sciences, Kangwon National University) ;
  • Han, Sang-Wook (Department of Integrative Plant Science, Chung-Ang University) ;
  • Hong, Jeum Kyu (Department of Horticultural Science, Gyeongnam National University of Science and Technology (GNTech))
  • Received : 2018.07.18
  • Accepted : 2018.09.10
  • Published : 2018.12.01


Two rhizobacteria Bacillus aryabhattai H26-2 and B. siamensis H30-3 were evaluated whether they are involved in stress tolerance against drought and high temperature as well as fungal infections in Chinese cabbage plants. Chinese cabbage seedlings cv. Ryeokgwang (spring cultivar) has shown better growth compared to cv. Buram-3-ho (autumn cultivar) under high temperature conditions in a greenhouse, whilst there was no difference in drought stress tolerance of the two cultivars. In vitro growth of B. aryabhattai H26-2 and B. siamensis H30-3 were differentially regulated under PEG 6000-induced drought stress at different growing temperatures (30, 40 and $50^{\circ}C$). Pretreatment with B. aryabhattai H26-2 and B. siamensis H30-3 enhanced the tolerance of Chinese cabbage seedlings to high temperature, but not to drought stress. It turns out that only B. siamensis H30-3 showed in vitro antifungal activities and in planta crop protection against two fungal pathogens Alternaria brassicicola and Colletotrichum higginsianum causing black spots and anthracnose on Chinese cabbage plants cv. Ryeokgwang, respectively. B. siamensis H30-3 brings several genes involved in production of cyclic lipopeptides in its genome and secreted hydrolytic enzymes like chitinase, protease and cellulase. B. siamensis H30-3 was found to produce siderophore, a high affinity iron-chelating compound. Expressions of BrChi1 and BrGST1 genes were up-regulated in Chinese cabbage leaves by B. siamensis H30-3. These findings suggest that integration of B. aryabhattai H26-2 and B. siamensis H30-3 in Chinese cabbage production system may increase productivity through improved plant growth under high temperature and crop protection against fungal pathogens.

E1PPBG_2018_v34n6_555_f0001.png 이미지

Fig. 1. Different sensitivity of two Chinese cabbage seedlings (cvs. Ryeokgwang and Buram-3-ho) to high temperature and/or drought stress under greenhouse conditions. (A) Plant growth of two cultivars grown for five weeks after planting at four different planting dates (4 Jul, 4 Aug, 5 Sep and 5 Oct) under a plastic greenhouse condition. Changes in average maximum (Tmax), average mean (Tmean) and average minimal (Tmin) temperatures (℃) for five weeks under the greenhouse conditions were demonstrated. (B) Plant growth of two Chinese cabbage cultivars by stopping irrigations. Three-week-old seedlings were undergone different irrigation regimes for additional two-weeks. Error bars represent the standard errors of the means of the four independent experimental replications. Means followed by the same letter are not significantly different at 5% level by least significant difference test.

E1PPBG_2018_v34n6_555_f0002.png 이미지

Fig. 2. Bacterial tolerance to dehydration at different growing temperatures during in vitro liquid cultures. Two Bacillus species (B. aryabhattai H26-2 and B. siamensis H30-3) and two phytopathogenic bacteria Pectobacterium carotovorum subsp. carotovorum (Pcc) strain PCC21 and Xanthomonas campestris pv. campestris (Xcc) strain 8004 were cultured with increasing concentration (0, 4, 12 and 20%) of polyethylene glycol (PEG) 6000 at different temperatures (30, 40 and 50℃) for 48 h. Bacterial numbers were initially inoculated with 105 cfu/ml and indirectly measured using a spectrophotometer with optical density at 600 nm. Error bars represent the standard errors of the means of the four independent experimental replications. Means followed by the same letter are not significantly different at 5% level by least significant difference test.

E1PPBG_2018_v34n6_555_f0003.png 이미지

Fig. 3. Effect of pretreatment with rhizobacteria on growth of Chinese cabbage seedling (cvs. Ryeokgwang and Buram-3-ho) under drought stress at two different temperatures. Two-weekold seedlings were treated with Bacillus aryabhattai H26-2 and B. siamensis H30-3 for one week and then undergone different concentrations (0, 2 and 4%) of polyethylene glycol (PEG) 6000-mediated drought stresses under two growth temperature regimes. The seedlings were sub-irrigated with water as mocks. Fresh weight (g) of the seedlings was measured after 12 days and 5 days for normal and high temperature conditions, respectively. Error bars represent the standard errors of the means of the four independent experimental replications. Means followed by the same letter are not significantly different at 5% level by least significant difference test.

E1PPBG_2018_v34n6_555_f0004.png 이미지

Fig. 4. Protective effects of Bacillus siamensis H30-3 against fungal pathogens on Chinese cabbage plants. (A) Dual culture assay for in vitro inhibition of mycelial growth of Alternaria brassicicola and Colletotrichum higginsianum by B. siamensis H30-3. The fungal pathogens were co-cultured with the bacterial strain H30-3 for 15 and 12 days at 25℃ for A. brassicicola and C. higginsianum, respectively. (B) Inhibitory mycelial growth measured by half of the fungal colony diameter after co-culture. Error bars represent the standard errors of the means of the six independent experimental replications. Asterisks indicate significant differences as determined by Student’s t-test (P < 0.05). (C) Reduced black spot and anthracnose disease severities on Chinese cabbage plants by the antagonistic B. siamensis H30-3. Bacterial suspension (109 cfu/ml) of B. siamensis H30-3 was foliar sprayed at 1 day prior to challenge inoculations of the fungal pathogens. Disease severities were evaluated at 4 days after fungal inoculation based on 0-5 scales. Error bars represent the standard errors of the means of the four independent experimental replications. Means followed by the same letter are not significantly different at 5% level by least significant difference test.

E1PPBG_2018_v34n6_555_f0005.png 이미지

Fig. 5. Antifungal metabolites production and induced defence response of Chinese cabbage plants by Bacillus siamensis H30-3. (A) PCR-based detection of bacterial genes encoding antimicrobial lipopeptides from B. aryabhattai H26-2 and B. siamensis H30-3 genomes. M, DNA size marker. bacD, bacilysin; bmyA, bacillomycin; fenD, fengycin; ituA, iturin A; srfA, surfactin; zwiA, zwittermicin A. (B) Characteristics of hydrolytic enzyme secretion, siderophore production and phosphate (P)-solubilisation originated from B. siamensis H30-3. In vitro productions of chitinase, protease and cellulase by B. siamensis H30-3 were examined on different agar media described in Materials and methods. (C) Expression of defence-related genes in Chinese cabbage leaves treated with B. siamensis H30-3. Expression of basic glucanase 2 gene BrBGL2, chitinase 1 gene BrChi1, glutathione-S-transferase 1 gene BrGST1 and ascorbate peroxidase 1 gene BrAPX1 was analyzed by semi-quantitative RT-PCR technique. BrActin7 was used as an internal control. The number of PCR cycles of each result is indicated within the right parenthesis.


Supported by : Rural Development Administration


  1. Abd_Allah, E. F., Alqarawi, A. A., Hashem, A., Radhakrishnan, R., Al-Huqail, A. A., Al-Otibi, F. O. N., Malik, J. A., Alharbi, R. I. and Egamberdieva, D. 2017. Endophytic bacterium Bacillus subtilis (BERA 71) improves salt tolerance in chickpea plants by regulating the plant defense mechanisms. J. Plant Interact. 13:37-44.
  2. Ahmad, Z., Wu, J., Chen, L. and Dong, W. 2017. Isolated Bacillus subtilis strain 330-2 and its antagonistic genes identified by the removing PCR. Sci. Rep. 7:1777.
  3. Alamri, S. A. 2015. Enhancing the efficiency of the bioagent Bacillus subtilis JF419701 against soil-borne phytopathogens by increasing the productivity of fungal cell wall degrading enzymes. Arch. Phytopathol. Plant Protect. 48:159-170.
  4. Ali, S. Z., Sandhya, V., Grover, M., Kishore, N., Venkateswar Rao, L. and Venkateswarlu, B. 2009. Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol. Fertil. Soils 46:45-55.
  5. Ali, S. Z., Sandhya, V., Grover, M., Venkateswar Rao, L. and Venkateswarlu, B. 2011. Effect of inoculation with a thermotolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. J. Plant Interact. 6:239-246.
  6. Angadi, S. V., Cutforth, H. W., Miller, P. R., McConkey, B. G., Entz, M. H., Brandt, S. A. and Volkmar, K. M. 2000. Response of three Brassica species to high temperature stress during reproductive growth. Can. J. Plant Sci. 80:693-701.
  7. Asari, S., Matzen, S., Petersen, M. A., Bejai, S. and Meijer, J. 2016. Multiple effects of Bacillus amyloliquefaciens volatile compounds: plant growth promotion and growth inhibition of phytopathogens. FEMS Microbiol. Ecol. 92:fiw070.
  8. Asari, S., Ongena, M., Debois, D., De Pauw, E., Chen, K., Bejai, S. and Meijer, J. 2017. Insights into the molecular basis of biocontrol of Brassica pathogens by Bacillus amyloliquefaciens UCMB5113 lipopeptides. Ann. Bot. 120:551-562.
  9. Dixon, D. P., Lapthorn, A. and Edwards, R. 2002. Plant glutathione transferases. Genome Biol. 3:3004.1-3004.10.
  10. Dong, X., Yi, H., Lee, J., Nou, I. S., Han, C. T. and Hur, Y. 2015. Global gene-expression analysis to identify differentially expressed genes critical for the heat stress response in Brassica rapa. PLoS One 10:e0130451.
  11. Duijff, B. J., Meijer, J. W., Bakker, P. A. H. M. and Schippers, B. 1993. Siderophore-mediated competition for iron and induced resistance in the suppression of fusarium wilt of carnation by fluorescent Pseudomonas spp. Neth. J. Plant Pathol. 99:277-289.
  12. Elad, Y. and Pertot, I. 2014. Climate change impacts on plant pathogens and plant diseases. J. Crop Improv. 28:99-139.
  13. Fahad, S., Bajwa, A. A., Nazir, U., Anjum. S. A., Farooq, A., Zohaib, A., Sadia, S., Nasim, W., Adkins, S., Saud, S., Ihsan, M. Z., Alharby, H., Wu, C., Wang, D. and Huang, J. 2017. Crop production under drought and heat stress: plant responses and management options. Front. Plant Sci. 8:1147.
  14. Fincheira, P. and Quiroz, A. 2018. Microbial volatiles as plant growth inducers. Microbiol. Res. 208:63-75.
  15. Gregory, P. J., Johnson, S. N., Newton, A. C. and Ingram, J. S. 2009. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60:2827-2838.
  16. Han, J.-H., Shim, H., Shin, J.-H. and Kim, K. S. 2015. Antagonistic activities of Bacillus spp. strains isolated from tidal flat sediment towards anthracnose pathogens Colletotrichum acutatum and C. gloeosporioides in South Korea. Plant Pathol. J. 31:165-175.
  17. Han, J.-H., Park, G.-C. and Kim, K. S. 2017. Antagonistic evaluation of Chromobacterium sp. JH7 for biological control of ginseng root rot caused by Cylindrocarpon destructans. Mycobiololgy 45:370-378.
  18. Jeong, H., Jeong, D.-E., Kim, S. H., Song, G. C., Park, S.-Y., Ryu, C.-M., Park, S.-H. and Choi, S.-K. 2012. Draft genome sequence of the plant growth-promoting bacterium Bacillus siamensis KCTC $13613^T$. J. Bacteriol. 194:4148-4149.
  19. Kakar, K. U., Ren, X.-L., Nawaz, Z., Cui, Z.-Q., Li, B., Xie, G.-L., Hassan, M. A., Ali, E. and Sun, G.-C. 2016. A consortium of rhizobacterial strains and biochemical growth elicitors improve cold and drought stress tolerance in rice (Oryza sativa L.). Plant Biol. 18:471-483.
  20. Kang, S.-M., Radhakrishnan, R. and Lee, I. J. 2015. Bacillus amyloliquefaciens subsp. plantarum GR53, a potent biocontrol agent resists Rhizoctonia disease on Chinese cabbage through hormonal and antioxidants regulation. World J. Microbiol. Biotechnol. 31:1517-1527.
  21. Kask, K., Kannaste, A., Talts, E., Copolovici, L. and Niinemets, U. 2016. How specialized volatiles respond to chronic and shortterm physiological and shock heat stress in Brassica nigra. Plant Cell Environ. 39:2027-2042.
  22. Kavamura, V. N., Santos, S. N., da Silva, J. L., Parma, M. M., Avila, L. A., Visconti, A., Zucchi, T. D., Taketani, R. G., Andreote, F. D. and de Melo, I. S. 2013. Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol. Res. 168:183-191.
  23. Kim, B.-R., Park, M.-S., Han, K.-S., Hahm, S.-S., Park, I.-H. and Song, J.-K. 2018. Biological control using Bacillus toyonensis strain CAB12243-2 against soft rot on Chinese cabbage. Korean J. Organic Agric. 26:129-140.
  24. Kim, J.-S., Lee, J., Lee, C.-H., Woo, S. W., Kang, H., Seo, S.-G. and Kim, S.-H. 2015a. Activation of pathogenesis-related genes by the rhizobacterium, Bacillus sp. JS, which induces systemic resistance in tobacco plants. Plant Pathol. J. 31:195-201.
  25. Kim, S. Y., Sang, M. K., Weon, H.-Y., Jeon, Y.-A., Ryoo, J. H. and Song, J. 2016. Characterization of multifunctional Bacillus sp. GH1-13. Korean J. Pestic. Sci. 20:189-196 (in Korean).
  26. Kim, Y. J., Lee, Y. H., Lee, H.-J., Jung, H. and Hong, J. K. 2015b. $H_2O_2$ production and gene expression of antioxidant enzymes in kimchi cabbage (Brassica rapa var. glabra Regel) seedlings regulated by plant development and nitrosative stresstriggered cell death. Plant Biotechnol. Rep. 9:67-78.
  27. Kim, Y.-W., Jung, H.-J., Park, J.-I., Hur, Y. and Nou, I.-S. 2015c. Response of NBS encoding resistance genes linked to both heat and fungal stress in Brassica oleracea. Plant Physiol. Biochem. 86:130-136.
  28. Lee, S. G., Lee, H. J., Kim, S. K., Choi, C. S., Park, S. T., Jang, Y. A. and Do, K. R. 2015. Effects of vernalization, temperature, and soil drying periods on the growth and yield of Chinese cabbage. Korean J. Hortic. Sci. Technol. 33:820-828.
  29. Lee, S. G., Lee, H. J., Kim, S. K., Choi, C. S. and Park, S. T. 2016. Influence of waterlogging period on the growth, physiological responses, and yield of kimchi cabbage. J. Environ. Sci. Int. 25:535-542 (in Korean).
  30. Lee, Y. H. and Hong, J. K. 2012. Host and non-host resistance of kimchi cabbage against different Xanthomonas campestris pathovars. Plant Pathol. J. 28:322-329.
  31. Lee, Y. H. and Hong, J. K. 2014. Differential defence responses of susceptible and resistant kimchi cabbage cultivars to anthracnose, black spot and black rot diseases. Plant Pathol. 64:406-415.
  32. Lim, J.-H. and Kim, S.-D. 2013. Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol. J. 29:201-208.
  33. Maksimov, I. V., Abizgil'dina, R. R. and Pusenkova, L. I. 2011. Plant growth promoting rhizobacteria as alternative to chemical crop protectors from pathogens (Review). Appl. Biochem. Microbiol. 47:333-345.
  34. Nautiyal, C. S., Srivastava, S., Chauhan, P. S., Seem, K., Mishra, A. and Sopory, S. K. 2013. Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profiles of leaf and rhizosphere community in rice during salt stress. Plant Physiol. Biochem. 66:1-9.
  35. Neeraja, C., Anil, K., Purushotham, P., Suma, K., Sarma, P. V. S. R. N., Moerschbacher, B. M. and Podile, A. R. 2010. Biotechnological approaches to develop bacterial chitinases as a bioshield against fungal diseases of plants. Crit. Rev. Biotechnol. 30:231-241.
  36. Ngumbi, E. and Kloepper, J. 2016. Bacterial-mediated drought tolerance: Current and future prospects. Appl. Soil Ecol. 105:109-125.
  37. Oh, S., Moon, K. H., Son, I.-C., Song, E. Y., Moon, Y. E. and Koh, S. C. 2014. Growth, photosynthesis and chlorophyll fluorescence of Chinese cabbage in response to high temperature. Korean J. Hort. Sci. Technol. 32:318-329. (in Korean)
  38. Ongena, M. and Jacques, P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trend Microbiol. 16:115-125.
  39. Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J.-L. and Thonart, P. 2007. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol. 9:1084-1090.
  40. Park, K., Ahn, I.-P. and Kim, C.-H. 2001. Systemic resistance and expression of the pathogenesis-related genes mediated by the plant growth-promoting rhizobacterium Bacillus amyloliquefaciens EXTN-1 against anthracnose disease in cucumber. Mycobiology 29:48-53.
  41. Park, T. -H., Choi, B. -S., Choi, A. -Y., Choi, I. -Y., Heu, S. and Park, B. -S. 2012. Genome sequence of Pectobacterium carotovorum subsp. carotovorum strain PCC21, a pathogen causing soft rot in Chinese cabbage. J. Bacteriol. 194:6345-6346.
  42. Park, Y.-G., Mun, B.-G., Kang, S.-M., Hussain, A., Shahzad, R., Seo, C.-W., Kim, A.-Y., Lee, S.-U., Oh, K. Y., Lee, D. Y., Lee, I.-J. and Yun, B. W. 2017. Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones. PLoS One 12:e0173203.
  43. Rakotoniriana, E. F., Rafamantanana, M., Randriamampionona, D., Rabemanantsoa, C., Urveg-Ratsimamanga, S., El Jaziri, M., Munaut, F., Corbisier, A.-M., Quetin-Leclercq, J. and Declerck, S. 2013. Study in vitro of the impact of endophytic bacteria isolated from Centella asiatica on the disease incidence caused by the hemibiotrophic fungus Colletotrichum higginsianum. Antonie Van Leeuwenhoek 103:121-133.
  44. Reyes-Ramirez, A., Escudero-Abarca, B. I., Aguilar-Uscanga, G., Hayward-Jones, P. M. and Barboza-Corona, J. E. 2004. Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. J. Food Sci. 69:M131-M134.
  45. Sammis, T. W., Kratky, B. A. and Wu, I. P. 1988. Effects of limited irrigation on lettuce and Chinese cabbage yields. Irrigation Sci. 9:187-198.
  46. Sang, M. K., Dutta, S. and Park, K. 2015. Influence of commercial antibiotics on biocontrol of soft rot and plant growth promotion in Chinese cabbages by Bacillus vallismortis EXTN-1 and BS07M. Res. Plant Dis. 21:255-260.
  47. Shafi, J., Tian, H. and Ji, M. 2017. Bacillus species as versatile weapons for plant pathogens: a review. Biotechnol. Biotechnol. Equip. 31:446-459.
  48. Sherriff, C. and Lucas, J. A. 1990. The host range of isolates of downy mildew, Peronospora parasitica, from Brassica crop species. Plant Pathol. 39:77-91.
  49. Slusarenko, A. J. and Schlaich, N. L. 2003. Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol. Plant Pathol. 4:159-170.
  50. Sulochana, M. B., Jayachandra, S. Y., Kumar, S. K. A. and Dayanand, A. 2014 Antifungal attributes of siderophore produced by the Pseudomonas aeruginosa JAS-25. J. Basic Microbiol. 54:418-424.
  51. Sun, C., Johnson, J. M., Cai, D., Sherameti, I., Oelmuller, R. and Lou, B. 2010. Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J. Plant Physiol. 167:1009-1017.
  52. Tahir, H. A. S., Gu, Q., Wu, H., Niu, Y., Huo, R. and Gao, X. 2017. Bacillus volatiles adversely affect physiology and ultrastructure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci. Rep. 7:40481.
  53. Templer, S. E., Ammon, A., Pscheidt, D., Ciobotea, O., Schuy, C., McCollum, C., Sonnewald, U., Hanemann, A., Forster, J., Ordon, F., von Korff, M. and Voll, L. M. 2017. Metabolite profiling of barley flag leaves under drought and combined heat and drought stress reveals metabolite QTLs for metabolites associated with antioxidant defense. J. Exp. Bot. 68:1697-1713.
  54. Timmusk, S., Abd El-Daim, I. A., Copolovici, L., Tanilas, T., Kannaste, A., Behers, L., Nevo, E., Seisenbaeva, G., Stenstrom, E. and Niinemets, U. 2014. Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: Enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9:e96086.
  55. Wang, C.-J., Yang, W., Wang, C., Gu, C., Niu, D.-D., Liu, H.-X., Wang, Y.-P. and Guo, J.-H. 2012. Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 7:e52565.
  56. Wang, N., Liu, M., Guo, L., Yang, X. and Qiu, D. 2016. A novel protein elicitor (PeBA1) from Bacillus amyloliquefaciens NC6 induces systemic resistance in tobacco. Int. J. Biol. Sci. 12:757-767.
  57. Wilson, R. A., Sangha, M. K., Banga, S. S., Atwal, A. K. and Gupta, S. 2014. Heat stress tolerance in relation to oxidative stress and antioxidants in Brassica juncea. J. Environ. Biol. 35:383-387.
  58. Yan, M. 2015. Seed priming stimulate germination and early seedling growth of Chinese cabbage under drought stress. S. Afr. J. Bot. 99:88-92.
  59. Yang, Y.-W., Tsai, C.-C., Liou, T.-D. and Chen, K.-S. 2001. Two heat-tolerant F1 hybrids of Chinese cabbage. HortScience 36:1144-1145.
  60. Yang, J., Kloepper, J. W. and Ryu, C.-M. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14:1-4.
  61. Yoo, S.-J. and Sang, M. K. 2017. Induced systemic tolerance to multiple stresses including biotic and abiotic factors by rhizobacteria. Res. Plant Dis. 23:99-113 (in Korean).
  62. Zandalinas, S. I., Rivero, R. M., Martinez, V., Gomez-Cadenas, A. and Arbona, V. 2016. Tolerance of citrus plants to the combination of high temperatures and drought is associated to the increase in transpiration modulated by a reduction in abscisic acid levels. BMC Plant Biol. 16:105.
  63. Zhao, F., Zhang, D., Zhao, Y., Wang, W., Yang, H., Tai, F., Li, C. and Hu, X. 2016. The difference of physiological and proteomic changes in maize leaves adaptation to drought, heat and combined both stresses. Front. Plant Sci. 7:1471.
  64. Zhou, R., Yu, X., Ottosen, C.-O., Rosenqvist, E., Zhao, L., Wang, Y., Yu, W., Zhao, T. and Wu, Z. 2017. Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol. 17:24.