<i>Paenarthrobacter nitroguajacolicus</i> can promote cucumber growth and control cucumber corynespora leaf spot

doi:10.15302/J-FASE-2024537

Front. Agr. Sci. Eng.

2024, Vol. 11

Issue (3) : 485-498 https://doi.org/10.15302/J-FASE-2024537

Paenarthrobacter nitroguajacolicus can promote cucumber growth and control cucumber corynespora leaf spot

Min LI^1,², Yahui HUANG¹, Xiaomin DONG², Xu ZHANG³(

), Qing MA²(

)

¹. College of Horticulture, South China Agricultural University, Guangzhou 510642, China
². State Key Laboratory of Crop Stress Biology for Arid Areas/College of Plant Protection, Northwest A&F University, Yangling 712100, China
³. College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, China

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Abstract

● First report of bacteria Paenarthrobacter nitroguajacolicus for effective control of cucumber corynespora leaf spot and promotion of cucumber growth.

● P. nitroguajacolicus strain BJ-5 is well-adapted for biocontrol being tolerant of saline environments.

● P. nitroguajacolicus produces a variety of secondary metabolites that promote plant growth.

Currently, the disease control in cucumber mainly depends on agrochemicals, which is not an environmentally benign strategy. Biocontrol bacteria not only resist plant pathogens but also promote plant growth, which is ecofriendly and sustainable option. A biocontrol bacterial strain BJ-5 was screened using Corynespora cassiicola as the target pathogen, and BJ-5 was determined to be Paenarthrobacter nitroguajacolicus by morphological and molecular methods. The effect of BJ-5 on C. cassiicola was studied, including the spore germination, cell membrane permeability and infected cucumbers. BJ-5 inhibited the germination of C. cassiicola spores in vitro and led to atrophy and deformation of the C. cassiicola budding tubes. BJ-5 caused the relative extracellular conductivity of C. cassiicola mycelia to increase compared with the control. Additionally, BJ-5 reduced the severity of cucumber corynespora leaf spot of cucumber infected with C. cassiicola. The inhibition efficacy of BJ-5 suspension as a foliar spray against cucumber corynespora leaf spot reached 63% inhibition, which is higher than a 5000-fold dilution of Luna-Son SC fungicide. In addition, BJ-5 was tested on the emergence of cucumber seedlings, recording the biomass and photosynthesis of cucumber during the growth period. BJ-5 at 1.5 × 10⁵ CFU·mL⁻¹ promoted the germination of cucumber seeds and increased biomass and photosynthesis at the adult plant stage. Also, the secondary metabolites of BJ-5 were determined. BJ-5 could produce chitinases, siderophore, cellulase, amylase and protease in the respective medium. Finally, adaptation assay of BJ-5 showed good salt tolerance and good adaptability in alkaline conditions, and that BJ-5 retains inhibition of fungi activity at higher temperatures. This is the first report of the biocontrol by P. nitroguajacolicus with antagonism to C. cassiicola and promote cucumber growth. This study indicates that P. nitroguajacolicus may serve as potential biocontrol agents against cucumber corynespora leaf spot fungus.

Keywords Adaptability antagonistic bacterium disease resistance growth promotion secondary metabolite

Corresponding Author(s): Xu ZHANG,Qing MA

Just Accepted Date: 17 January 2024 Online First Date: 05 February 2024 Issue Date: 17 July 2024

Cite this article:

Min LI,Yahui HUANG,Xiaomin DONG, et al. Paenarthrobacter nitroguajacolicus can promote cucumber growth and control cucumber corynespora leaf spot[J]. Front. Agr. Sci. Eng. , 2024, 11(3): 485-498.

URL:

https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2024537
https://academic.hep.com.cn/fase/EN/Y2024/V11/I3/485

Fig.1 Introduction to cucumber corynespora leaf spot: (a) infection of cucumber with corynespora leaf spot in greenhouses; (b) diseased cucumber leaves; (c) morphological characteristics of condia of C. cassiicola; (d) colony morphology of C. cassiicola; (e) symptoms 7 days after inoculation of cucumber leaves; (f) polymerase chain reaction products of rDNA-ITS amplified 564 bp; and (g) phylogenetic tree constructed with Neighbor-Joining method based on the rDNA-ITS of C. cassiicola and other 21 related strains.

Fig.2 Screening and identification biocontrol bacteria: (a) confrontation results of different biocontrol bacteria against C. cassiicola in a dishes; (b) physiological and biochemical characteristics of BJ-5 (part)-gelatin liquefaction, tyrosine hydrolysis, ammonium production and Gram test in that order; (c) BJ-5 colony morphology; (d) polymerase chain reaction products of 16S rDNA amplified 1424 bp; and (e) phylogenetic tree constructed with Neighbor-Joining method based on the 16S rDNA of BJ-5 and 17 related strains.

Tab.1 Physiological and biochemical characteristics (positive (+) and negative (?) reactions) of Paenarthrobacter nitroguajacolicus strain BJ-5

Tab.2 Effects of Paenarthrobacter nitroguajacolicus strain BJ-5 on conidial germination of Corynespora cassiicola

Fig.3 Inhibit C. cassiicola by P. nitroguajacolicus strain BJ-5: (a) effect of BJ-5 on C. cassiicola spore germination; (b) determination of conductivity; (c) normal cucumber; (d) inoculated cucumbers with C. cassiicola; (e) 5000-fold dilution of Luna-Son SC (21.5% Trifloxystrobin and 21.5% Fluopyram) was used as the fungicide experimental group; and (f) 1 × 10⁸ CFU·mL^?1 of BJ-5 suspension apllied as a spray.

Tab.3 Control effect of Paenarthrobacter nitroguajacolicus strain BJ-5 on cucumber corynespora leaf disease

Fig.4 The growth promotion of cucumber by P. nitroguajacolicus strain BJ-5: (a) cucumber seeds treated with different concentrations of BJ-5 suspension; (b) germination rate of cucumber seeds soaked in BJ-5 suspension at different concentrations; (c) germination bag growth of cucumber seed biomass of BJ-5 suspension and sterile water for 10 days; (d) effects of BJ-5 on cucumber biomass; (e) control; (f) seeds treated with 1.5 × 10⁵ CFU·mL^?1 dilution of BJ-5 suspension; (g) seeds treated with 1.5 × 10⁶ CFU·mL^?1 dilution of BJ-5 suspension; and (h) effects of BJ-5 on photosynthesis in cucumber leaves.

Tab.4 Effects of Paenarthrobacter nitroguajacolicus strain BJ-5 on cucumber biomass

Fig.5 Detection of secondary metabolites and adaptation assay of P. nitroguajacolicus strain BJ-5: (a) secondary metabolites detection (enzyme secretion detection); (b) high temperature stability of the BJ-5 suspension; and (c) NaCl tolerance range of BJ-5; (d, e) pH tolerance range of BJ-5.

1	N N, Winstead L H, Person R D Riggs . Cercospora leaf spot on cucumbers in North Carolina. Plant Disease, 1957, 41(9): 794
2	A, Garibaldi S, Rapetti J, Rossi M L Gullino . First report of leaf spot caused by Corynespora cassiicola on Basil (Ocimum basilicum) in Italy. Plant Disease, 2007, 91(10): 1361 https://doi.org/10.1094/PDIS-91-10-1361B
3	L G, Sumabat R C Jr, Kemerait M T Brewer . Phylogenetic diversity and host specialization of Corynespora cassiicola responsible for emerging target spot disease of cotton and other crops in the southeastern United States. Phytopathology, 2018, 108(7): 892–901 https://doi.org/10.1094/PHYTO-12-17-0407-R
4	S, Wang H Liu . Identification of Corynespora cassiicola causing leaf spot on Syringa species. Forest Pathology, 2021, 51(3): e12684 https://doi.org/10.1111/efp.12684
5	X Y, Li M, Li H, Liu Z, Luo Y, Wang Q Ma . Identification of cucumber target spot fungus and determination of agent virulence in Shaanxi. Acta Agriculturae Boreali-occidentalis Sinica, 2023, 32(5): 807−814 (in Chinese)
6	M K, Kwon B R, Kang B H, Cho Y C Kim . Occurrence of target leaf spot disease caused by Corynespora cassicola on cucumber in Korea. Plant Pathology, 2003, 52(3): 424 https://doi.org/10.1046/j.1365-3059.2003.00846.x
7	D, Ma J, Jiang J, Zhu L, Zhang B, Li W, Mu F Liu . Evaluation of sensitivity and resistance risk of Corynespora cassiicola to isopyrazam and mefentrifluconazole. Plant Disease, 2020, 104(11): 2779–2785 https://doi.org/10.1094/PDIS-02-20-0384-RE
8	Y, Deng T, Wang P, Zhao Y, Du L, Zhang Z, Qi M Ji . Sensitivity to 12 fungicides and resistance mechanism to trifloxystrobin, carbendazim and SDHIs in cucumber Corynespora leaf spot (Corynespora cassiicola). Plant Disease, 2023, 107(12): 3782–3791 https://doi.org/10.1094/PDIS-04-23-0615-RE
9	M, Li Q, Ma H, Lei Y Wang . Occurrence and green control technology of cucumber target spot. Northwest Horticulture, 2020, (03): 40−41 (in Chinese)
10	S, Jisha P R, Gouri K N, Anith K K Sabu . Piriformospora indica cell wall extract as the best elicitor for asiaticoside production in Centella asiatica (L.) Urban, evidenced by morphological, physiological and molecular analyses. Plant Physiology and Biochemistry, 2018, 125: 106–115 https://doi.org/10.1016/j.plaphy.2018.01.021
11	S, Compant C, Clément A Sessitsch . Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biology & Biochemistry, 2010, 42(5): 669–678 https://doi.org/10.1016/j.soilbio.2009.11.024
12	R, Hernández-León D, Rojas-Solís M, Contreras-Pérez M C O, Mosqueda L I, Macías-Rodríguez la Cruz H R, de E, Valencia-Cantero G Santoyo . Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biological Control, 2015, 81: 83–92 https://doi.org/10.1016/j.biocontrol.2014.11.011
13	Y, Pii A, Penn R, Terzano C, Crecchio T, Mimmo S Cesco . Plant-microorganism-soil interactions influence the Fe availability in the rhizosphere of cucumber plants. Plant Physiology and Biochemistry, 2015, 87: 45–52 https://doi.org/10.1016/j.plaphy.2014.12.014
14	E, Ahmed S J M Holmström . Siderophores in environmental research: roles and applications. Microbial Biotechnology, 2014, 7(3): 196–208 https://doi.org/10.1111/1751-7915.12117
15	U, Chakraborty B N, Chakraborty A P, Chakraborty K Sunar . Plant growth promoting rhizobacteria mediated improvement of health status of tea plants. Indian Journal of Biotechnology, 2013, 12(1): 20–31
16	A, Aeron E, Khare C K, Jha V S, Meena S M A, Aziz M T, Islam K, Kim S K, Meena A, Pattanayak H, Rajashekara R C, Dubey B R, Maurya D K, Maheshwari M, Saraf M, Choudhary R, Verma H N, Meena A R N S, Subbanna M, Parihar S, Shukla G, Muthusamy R S, Bana V K, Bajpai Y K, Han M, Rahman D, Kumar N P, Singh R K Meena . Revisiting the plant growth-promoting rhizobacteria: lessons from the past and objectives for the future. Archives of Microbiology, 2020, 202(4): 665–676 https://doi.org/10.1007/s00203-019-01779-w
17	No Zhongnong . 6 Cucumber. Beijing: Institute of Vegetable and Flower Sciences, Chinese Academy of Agricultural Sciences, 2002 (in Chinese)
18	Daily Farmers’ . Bayer launches new fruit and vegetable fungicide Luna-Son. China Vegetables, 2014, (2): 47 (in Chinese)
19	B, Prapagdee C, Kuekulvong S Mongkolsuk . Antifungal potential of extracellular metabolites produced by Streptomyces hygroscopicus against phytopathogenic fungi. International Journal of Biological Sciences, 2008, 4(5): 330–337 https://doi.org/10.7150/ijbs.4.330
20	X Z, Dong M Y Cai . Manual for Identification of Common Bacterial Systems. Beijing: Science Press, 2001 (in Chinese)
21	Y J, Zhang D, Liu B Z, Ma X Y, Zhou D Miao . Investigation and pathogen identification of cucumber corynespora leaf spot in Heilongjiang Province. Journal of Northeast Agricultural University, 2014, 45(9): 34–39, 34 (in Chinese)
22	X J, Li K, Li D B, Zhou M Y, Zhang D F, Qi T, Jing X P, Zang C L, Qi W, Wang J H Xie . Biological control of banana wilt disease caused by Fusarium Oxyspoum f. sp. Cubense using Streptomyces sp. H4. Biological Control, 2021, 155: 104524 https://doi.org/10.1016/j.biocontrol.2020.104524
23	L M, Li T T, Zheng Y Q, Chen Y, Sui R H, Ding L W, Hou F L, Zheng C Y Zhu . The antagonistic mechanisms of Streptomyces sioyaensis on the growth and metabolism of poplar canker pathogen Valsa sordida. Biological Control, 2020, 151: 104392
24	X, Zhao X, Liu H, Zhao Y, Ni Q, Lian H, Qian B, He H, Liu Q Ma . Biological control of Fusarium wilt of sesame by Penicillium bilaiae 47M–1. Biological Control, 2021, 158: 104601 https://doi.org/10.1016/j.biocontrol.2021.104601
25	L V Madden . Botanical epidemiology: some key advances and its continuing role in disease management. European Journal of Plant Pathology, 2006, 115(1): 3–23 https://doi.org/10.1007/s10658-005-1229-5
26	L, He L, Yu B, Li N, Du S Guo . The effect of exogenous calcium on cucumber fruit quality, photosynthesis, chlorophyll fluorescence, and fast chlorophyll fluorescence during the fruiting period under hypoxic stress. BMC Plant Biology, 2018, 18(1): 180 https://doi.org/10.1186/s12870-018-1393-3
27	M, Li G, Ma H, Lian X, Su Y, Tian W, Huang J, Mei X Jiang . The effects of Trichoderma on preventing cucumber fusarium wilt and regulating cucumber physiology. Journal of Integrative Agriculture, 2019, 18(3): 607–617 https://doi.org/10.1016/S2095-3119(18)62057-X
28	H K, Awla J, Kadir R, Othman T S, Rashid S, Hamid M Y Wong . Plant growth-promoting abilities and biocontrol efficacy of Streptomyces sp. UPMRS4 against Pyricularia oryzae. Biological Control, 2017, 112: 55−63
29	B, Ma W, Song X, Zhang M, Chen J, Li X, Yang L Zhang . Potential application of novel cadmium-tolerant bacteria in bioremediation of Cd-contaminated soil. Ecotoxicology and Environmental Safety, 2023, 255: 114766 https://doi.org/10.1016/j.ecoenv.2023.114766
30	V, Riva F, Mapelli G, Dragonetti M, Elfahl L, Vergani P, Crepaldi Maddalena N, La S Borin . Bacterial inoculants mitigating water scarcity in tomato: the importance of long-term in vivo experiments. Frontiers in Microbiology, 2021, 12: 675552 https://doi.org/10.3389/fmicb.2021.675552
31	J H, Jang G, Sathiyaraj S, Sathiyaraj J W, Lee J Y, Kim S, Maeng K E, Lee E, Lee M S, Kang M K Kim . A report of eight unrecorded radiation resistant bacterial species in Korea isolated in 2018. Journal of Species Research, 2018, 7(3): 210–221
32	M T, Sherpa N, Bag S, Das P, Haokip L Sharma . Isolation and characterization of plant growth promoting rhizobacteria isolated from organically grown high yielding pole type native pea (Pisum sativum L.) variety Dentami of Sikkim, India. Current Research in Microbial Sciences, 2021, 2: 100068 https://doi.org/10.1016/j.crmicr.2021.100068
33	Y R, Zhao L, Li X W, Xie Y C, Shi A L, Chai G Y, Sun B J Li . Biocontrol effect of Bacillus velezensis strain ZF2 against Corynespora cassiicola. Chinese Journal of Biological Control, 2019, 35(2): 217−225 (in Chinese)
34	R S, Zhang X H, Dai Y F, Liu Z Y Chen . Promoting effect of Bacillus amylolivier Lx-11 on rice growth and analysis of growth-promoting substances. Journal of Nuclear Agricultural Sciences, 2018, 32(6): 1230−1238 (in Chinese)

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