Diversity and Efficacy Mold Rhizosphere to Control Lasiodiplodia theobromae Causing Stem-End Rot Disease on Citrus nobilis from East Kalimantan: Diversity and Efficacy Mold Rhizosphere to Control Lasiodiplodia theobromae

Nensi Agustina; Mutia Erti  Dwiastuti; Anang  Triwiratno; Suharjono

doi:10.11594/jtls.14.03.05

Authors

Nensi Agustina Brawijaya University
Mutia Erti Dwiastuti Agricultural Food Research Organization National Research and Innovation Agency of Indenesia
Anang Triwiratno Agricultural Food Research Organization, National Research and Innovation Agency of Indenesia
Suharjono Biology Departement, Brawijaya University

DOI:

https://doi.org/10.11594/jtls.14.03.05

Keywords:

Antagonist Agent, Diversity, Dual culture, Mono spore, Structural Equa-tion Modelling

Abstract

The current study aimed to determine the abundance and diversity of soil characteristics and their relationship with mold abundance and potential in inhibiting Lasiodiplodia theobromae, a potential rhizosphere mold species of Siamese orange plant. The pathogenic mold that causes stem-end rot disease was isolated from stems with rotting symptoms. In contrast, the antagonistic mold was obtained from isolation from the rhizosphere soil of Siamese plants. The samples were collected from Siamese orchards in East Kalimantan. The abundance and diversity of molds on swamp land are higher than on dry land. A total of 28 molds were found in the rhizosphere of Siamese orange plants. Mold abundance was positively correlated with soil moisture, organic matter, C-Organic, and N-total but negatively correlated with temperature and pH. Soil chemical characteristics directly influence mold abundance, while soil chemical characteristics indirectly influence it. 21 out of 28 isolates were Biological Control Agents (BCA). TR37 mold has the highest inhibitory power of 89.31% of the D13.C2 pathogen that causes stem-end rot disease. ITS rDNA sequence homology shows that the TR37 mold identified as Trichoderma reesei, while pathogen Lasiodiplodia theobromae causes stem-end rot disease

References

Sofiyanti N, Iriani D, Wahyuni PI, et al. (2022) Identification, Morphology of Citrus L. (Aurantioide-ae-Rutaceae Juss.) and its Traditional uses in Riau Province, Indonesia. Biodiversitas J Biol Divers. doi: 10.13057/biodiv/d230247

Nian RH Poerwanto R, Suketi K (2016) Degreening Buah Jeruk Siam (Citrus nobilis) pada Beberapa Konsentrasi dan Durasi Pemaparan Etilen. Jurnal Hortikultura Indonesia 7 (2): 111–120. doi: 10.29244/jhi.7.2.111-120.

Julaeha E, Dewi KS, Nurzaman M, et al. (2020) Chemical Compositions and Antioxidant Activities of Indonesian Citrus Essential Oils and Their Elucidation Using Principal Component Analysis. doi: 10.20944/preprints202011.0586.v1

Lv X, Zhao S, Ning Z, et al. (2015) Citrus Fruits as a Treasure Trove of Active Natural Metabolites that Potentially Provide Benefits for Human Health. Chemistry Central Journal 9 (1): 68. doi: 10.1186/s13065-015-0145-9.

Aini N, Dwiyanti H, Setyawati R, et al. (2022) Siam Orange (Citrus nobilis L.) Nectar Characteristics with Variations Instabilizer and Sucrose Level. Food Research 6 (3): 315–323. doi: 10.26656/fr.2017.6(3).386.

Devy NF, Yulianti Y, Andrini A (2010) Kandungan Flavonoid Dan Limonoid Pada Berbagai Fase Per-tumbuhan Tanaman Jeruk Kalamondin (Citrus Mitis Blanco) Dan Purut (Citrus Hystrix Dc.). Jurnal Hortikultura 20 (1): 85292. doi: 10.21082/jhort.v20n1.2010.p%p.

Kementan (2017) Petunjuk Teknis Pengembangan Kawasan Tanaman Pangan. Direktorat Jendral Tanaman Pangan Kementerian Pertanian.

Zhang J (2014) Lasiodiplodia theobromae in Citrus Fruit (Diplodia Stem-End Rot). In: Postharvest Decay. Elsevier. pp 309–335.

Polanco-Florián LG, Alvarado-Gómez OG, Olivares-Sáenz E, et al. (2020) Biological Control of Lasiodip-lodia theobromae and Fomitopsis meliae causing the Regressive Death of Citrus. Revista Mexicana Cien-cias Agrícolas 11 (5): 1069–1081.

Gnanesh BN, Arunakumar GS, Tejaswi A, et al. (2022) Characterization and Pathogenicity of La-siodiplodia theobromae Causing Black Root Rot and Identification of Novel Sources of Resistance in Mul-berry Collections. The Plant Pathology Journal 38 (4): 272–286. doi: 10.5423/PPJ.OA.01.2022.0005.

Mirsam H, Kalqutny SH, Suriani, et al. (2021) Indigenous Fungi from Corn as a Potential Plant Growth Promoter and its Role in Fusarium verticil-lipids Suppression on Corn. Heliyon 7 (9): e07926. doi: 10.1016/j.heliyon.2021.e07926.

Yunus F, Lambui O, Suwastika IN (2017) Kelimpahan Mikroorganisme Tanah pada Sistem Perkebunan Kakao (Theobroma cacao L.) Semi In-tensif Dan Non Intensif. Nat Sci J Sci Technol. doi: 10.22487/25411969.2017.v6.i3.9192

Liang S, Arraiano-Castilho R, Neuenkamp L, et al. (2023) Rhizosphere Fungal Community Assembly Varied Across Functional Guilds in a Temperate For-est. Ecological Processes 12 (1): 6. doi: 10.1186/s13717-023-00417-0.

Wang Z, Li T, Wen X, et al. (2017) Fungal Communities in Rhizosphere Soil under Conserva-tion Tillage Shift in Response to Plant Growth. Fron-tiers in Microbiology 8 1301. doi: 10.3389/fmicb.2017.01301.

Kennedy AC, De Luna LZ (2005) RHIZO-SPHERE. In: Encycl. Soils Environ. Elsevier. pp 399–406.

Murali M, Naziya B, Ansari MA, et al. (2021) Bioprospecting of Rhizosphere-Resident Fungi: Their Role and Importance in Sustainable Agriculture. Journal of Fungi 7 (4): 314. doi: 10.3390/jof7040314.

Susanna, Sinaga MS, Wiyono S, Triwidodo H (2018) Pemanfaatan Cendawan Antagonis In Situ sebagai Agens Biokontrol Lasiodiplodia theobromae Penyebab Dieback pada Pala di Aceh Selatan. Jurnal Pertanian Tropik 5 (3): 447–454. doi: 10.32734/jpt.v5i3.3119.

Triasih U- (2020) Potency of Trichoderma sp., Antagonistic Fungi Derived from Soil Rhizospere, against Two Pathogens: Botryodiplodia theobromae Pat. and Fusarium sp. Wilt in Vitro. Gontor AGRO-TECH Science Journal 6 (2): 115. doi: 10.21111/agrotech.v6i2.4020.

Bhadra M, Khair A, Hossain MA, Sikder MM (2015) Efficacy of Trichoderma spp. and fungicides against Lasiodiplodia theobromae. Bangladesh Jour-nal of Scientific and Industrial Research 49 (2): 125–130. doi: 10.3329/bjsir.v49i2.22008.

Hassan N, Rafiq M, Rehman M, et al. (2019) Fungi in Acidic Fire: A Potential Source of Industrial-ly Important Enzymes. Fungal Biology Reviews 33 (1): 58–71. doi: 10.1016/j.fbr.2018.08.002.

Sari DNR, Anitasari SD (2022) Isolation of In-digenous Fungi in River Containing Ammonia from Rubber Industry Waste in Jember. Journal of Multi-disciplinary Applied Natural Science 2 (1): 58–64. doi: 10.47352/jmans.2774-3047.109.

Suharjono S, Kurniati TH, Soejono S, Dewi S (2019) Uji Antagonis Trichoderma sp dan Gliocladi-um sp terhadap Fusarium Penyebab Penyakit Layu pada Beberapa Jenis Tanaman Pisang di Kebun Raya Purwodadi secara in-vitro. Biota : Jurnal Ilmiah Ilmu-Ilmu Hayati 119–124. doi: 10.24002/biota.v9i2.2900.

Mailafia S, Okoh GR, Olabode HOK, Osanupin R (2016) Isolation and Identification of Fungi Associ-ated with Spoilt Fruits Vended in Gwagwalada Mar-ket, Abuja, Nigeria. Veterinary World 10 (4): 393–397. doi: 10.14202/vetworld.2017.393-397.

Yolcubal I, Brusseau ML, Artiola JF, et al. (2004) Environmental Physical Properties and Pro-cesses. USA, Elsevier.

FAO (2021) Standard Operating Procedure for Soil pH Determination. Rome, Italy, Food and Agri-culture Organization of the United Nations.

Ogundare MO, Lajide L (2013) Physico-Chemical and Mineral Analysis of Composts Fortified with NPK Fertilizer, Ammonium Chloride and Kaolin. Journal of Agricultural Chemistry and Environment 02 (02): 27–33. doi: 10.4236/jacen.2013.22005.

FAO (2023) Standard Operation Procedure for Soil Mosture Content by Gravimetric Method. Rome, Italy, Food and Agriculture Organization of the Unit-ed Nations.

FAO (2019) Standard operating procedure for soil organic carbon. Walkley-Black method: titration and colorimetric method. Rome, Italy, Food and Agriculture Organization of the United Nations.

FAO (2021) Standard Operating Procedure for Soil Nitrogen - Kjeldahl Method. Rome, Italy, Food and Agriculture Organization of the United Nations.

Khuong NQ, Nhien DB, Thu LTM, et al. (2023) Using Trichoderma asperellum to Antagonize Lasiodiplodia theobromae Causing Stem-End Rot Dis-ease on Pomelo (Citrus maxima). Journal of Fungi 9 (10): 981. doi: 10.3390/jof9100981.

Zymo Research (2021) Quick-DNATM Fun-gal/Bacterial Miniprep Kit.

Martin KJ, Rygiewicz PT (2005) Fungal-specific PCR Primers Developed for Analysis of the ITS Region of Environmental DNA Extracts. BMC Microbiology 5 (1): 28. doi: 10.1186/1471-2180-5-28.

Nishizawa T, Zhaorigetu, Komatsuzaki M, et al. (2010) Molecular Characterization of Fungal Communities in Non-Tilled, Cover-Cropped Upland Rice Field Soils. Microbes and Environments 25 (3): 204–210. doi: 10.1264/jsme2.ME10108.

De Castro O, Avino M, Di Maio A, et al. (2018) Sanger and Next Generation Sequencing in the Characterisation of Arbuscular Mycorrhizal Fungi (AMF) in Pancratium maritimum L. (Amaryllida-ceae), a Representative Plant Species of Mediterranean Sand Dunes. Planta 248 (6): 1443–1453. doi: 10.1007/s00425-018-2981-z.

Hishe S, Lyimo J, Bewket W (2017) Soil and Water Conservation Effects on Soil Properties in the Middle Silluh Valley, Northern Ethiopia. International Soil and Water Conservation Research 5 (3): 231–240. doi: 10.1016/j.iswcr.2017.06.005.

Nan J, Chao L, Ma X, et al. (2020) Microbial Diversity in the Rhizosphere Soils of Three Stipa Species from the Eastern Inner Mongolian Grasslands. Global Ecology and Conservation 22 e00992. doi: 10.1016/j.gecco.2020.e00992.

Abdel-Fattah MK, Mohamed ES, Wagdi EM, et al. (2021) Quantitative Evaluation of Soil Quality Us-ing Principal Component Analysis: The Case Study of El-Fayoum Depression Egypt. Sustainability 13 (4): 1824. doi: 10.3390/su13041824.

Martín-Sanz JP, De Santiago-Martín A, Valverde-Asenjo I, et al. (2022) Comparison of Soil Quality Indexes Calculated by Network and Principal Component Analysis for Carbonated Soils under Dif-ferent uses. Ecological Indicators 143 109374. doi: 10.1016/j.ecolind.2022.109374.

Strom N, Hu W, Haarith D, et al. (2020) Inter-actions Between Soil Properties, Fungal Communi-ties, the Soybean Cyst Nematode, and Crop Yield under Continuous Corn and Soybean Monoculture. Applied Soil Ecology 147 103388. doi: 10.1016/j.apsoil.2019.103388.

Yao R, Yang J, Zhu W, et al. (2021) Impact of Crop Cultivation, Nitrogen and Fulvic Acid on Soil Fungal Community Structure in Salt-affected Alluvial Fluvo-aquic Soil. Plant and Soil 464 (1–2): 539–558. doi: 10.1007/s11104-021-04979-w.

Dharanendra Swamy S, Mahadevakumar S, Vasanthkumar T, et al. (2020) First Report of La-siodiplodia pseudotheobromae Associated with Post Flowering Stalk Rot of Maize (Zea mays) from India. Plant Disease 104 (9): 2524. doi: 10.1094/PDIS-11-19-2418-PDN.

Tamura K, Nei M, Kumar S (2004) Prospects for Inferring Very Large Phylogenies by using the Neighbor-Joining Method. Proceedings of the National Academy of Sciences 101 (30): 11030–11035. doi: 10.1073/pnas.0404206101.

Broeckling CD, Paschke MW, Vivanco JM, Man-ter D (2008) Rhizosphere Ecology. In: Encycl. Ecol. Elsevier. pp 3030–3035.

Janowski D, Leski T (2022) Factors in the Distribution of Mycorrhizal and Soil Fungi. Diversity 14 (12): 1122. doi: 10.3390/d14121122.

Johansson P, Bok G, Ekstrand-Tobin A (2013) The Effect of Cyclic Moisture and Temperature on Mould Growth on Wood Compared to Steady State Conditions. Building and Environment 65 178–184. doi: 10.1016/j.buildenv.2013.04.004.

Muneer MA, Huang X, Hou W, et al. (2021) Response of Fungal Diversity, Community Composition, and Functions to Nutrients Management in Red Soil. Journal of Fungi 7 (7): 554. doi: 10.3390/jof7070554.

Ali WA, Hussein RH, Radef WT (2021) The Effect of Soil Properties on the Biological Diversity of Fungi in Soil University of Anbar. Journal of Physics: Conference Series 2114 (1): 1–7. doi: 10.1088/1742-6596/2114/1/012068.

De Vries FT, Hoffland E, Van Eekeren N, et al. (2006) Fungal/ Bacterial Ratios in Grasslands with Contrasting Nitrogen Management. Soil Biology and Biochemistry 38 (8): 2092–2103. doi: 10.1016/j.soilbio.2006.01.008.

Craswell ET, Lefroy RDB (2001) The role and function of organic matter in tropical soils. Nutrient Cycling in Agroecosystems 61 (1): 7–18. doi: 10.1023/A:1013656024633.

Prashar P, Kapoor N, Sachdeva S (2014) Rhizosphere: its Structure, Bacterial Diversity and Significance. Reviews in Environmental Science and Bio/Technology 13 (1): 63–77. doi: 10.1007/s11157-013-9317-z.

Arifah F, Aini LQ, Muhibuddin A (2023) Molecular and morphological characterization of fungi isolated from nutmeg (Myristica fragrans) in North Sulawesi, Indonesia. Biodiversitas J Biol Divers. doi: 10.13057/biodiv/d240151

Polihito RA (2022) Hubungan Kekerabatan Fenetik Lima Anggota Familia Araceae. Biosf J Biol Dan Pendidik Biol. doi: 10.23969/biosfer.v7i2.6120

Luo X, Liu K, Shen Y, et al. (2021) Fungal Community Composition and Diversity Vary With Soil Horizons in a Subtropical Forest. Frontiers in Microbiology 12 650440. doi: 10.3389/fmicb.2021.650440.

Zhang T, Wang N-F, Liu H-Y, et al. (2016) Soil pH is a Key Determinant of Soil Fungal Community Composition in the Ny-Ålesund Region, Svalbard (High Arctic). Frontiers in Microbiology 7 (227): 1–10. doi: 10.3389/fmicb.2016.00227.

Ismail MH, Fuad MFA, Zaki P, Jemali NJN (2017) Analysis of Importance Value Index of Un-logged and Logged Peat Swamp Forest in Nenasi Forest Reserve, Peninsular Malaysia. Bonorowo Wet-lands 7 (2): 74–78. doi: 10.13057/bonorowo/w070203.

de Melo NA, Delevati DM, da Costa A Ben, Lobo EA (2021) The use of Phytosociology to Evaluate the Efficiency of Headwater Preservation Areas in the Andreas Stream Hydrographic Basin, RS, Brazil. Ecological Indicators 129 1–7. doi: 10.1016/j.ecolind.2021.107904.

Liu KL, Chen BY, Zhang B, et al. (2023) Under-story Vegetation Diversity, Soil Properties and Microbial Community Response to Different Thinning Intensities in Cryptomeria japonica var. sinensis Plantations. Frontiers in Microbiology 14 (February): 1–13. doi: 10.3389/fmicb.2023.1117384.

Deng Z, Wang Y, Xiao C, et al. (2022) Effects of Plant Fine Root Functional Traits and Soil Nutrients on the Diversity of Rhizosphere Microbial Communi-ties in Tropical Cloud Forests in a Dry Season. For-ests 13 (421): 1–14. doi: 10.3390/f13030421.

Jia T, Yao Y, Guo T, et al. (2020) Effects of Plant and Soil Characteristics on Phyllosphere and Rhizosphere Fungal Communities During Plant Development in a Copper Tailings Dam. Frontiers in Microbiology 11 1–11. doi: 10.3389/fmicb.2020.556002.

Wei S, Liu B, Ni K, et al. (2023) Rhizosphere Microbial Community Shows a Greater Response Than Soil Properties to Tea (Camellia sinensis L.) Cultivars. Agronomy 13 (1): 1–17. doi: 10.3390/agronomy13010221.

Xiao D, Huang Y, Feng S, et al. (2018) Soil Organic Carbon Mineralization with Fresh Organic Substrate and Inorganic Carbon Additions in a red soil is controlled by Fungal Diversity along a pH Gradient. Geoderma 321 (December 2017): 79–89. doi: 10.1016/j.geoderma.2018.02.003.

Deltedesco E, Keiblinger KM, Piepho H-P, et al. (2023) Soil Microbial Community Structure and Function Mainly Respond to Indirect Effects in a Multifactorial Climate Manipulation Experiment. Journal of Fungi 9 (549): 1–19. doi: 10.1016/j.soilbio.2020.107704.

Bárcenas‐Moreno G, Gómez‐Brandón M, Rousk J, Bååth E (2009) Adaptation of Soil Microbial Com-munities to Temperature: Comparison of Fungi and Bacteria in a Laboratory Experiment. Global Change Biology 15 (12): 2950–2957. doi: 10.1111/j.1365-2486.2009.01882.x.

Chen X, Wang Y, Wang Y, et al. (2023) A Natural Moisture Gradient Affects Soil Fungal Communities on the South Shore of Hulun Lake, Inner Mongolia, China. Journal of Fungi 9 (5): 549. doi: 10.3390/jof9050549.

Ratnasari JD, Isnawati, Ratnasari E (2014) Uji Antagonis Cendawan Agens Hayati terhadap Cend-awan Cercospora musae Penyebab Penyakit Sigatoka secara In Vitro. Lentera Bio 3 (2): 129–135.

Thambugala KM, Daranagama DA, Phillips AJL, et al. (2020) Fungi vs. Fungi in Biocontrol: An Over-view of Fungal Antagonists Applied Against Fungal Plant Pathogens. Frontiers in Cellular and Infection Microbiology 10 (604923): 1–19. doi: 10.3389/fcimb.2020.604923.

Brito FDS, Costa DPD, Souza CAFD, et al. (2022) Selection and control efficacy of Trichoderma spp. against Fusarium solani and Lasiodiplodia theo-bromae causing root rot in forage cactus. Physiological and Molecular Plant Pathology 122 101900. doi: 10.1016/j.pmpp.2022.101900.

Anafarida O (2020) Analisis Filogenetik Mang-ga (Mangifera spp.) Berdasarkan Gen 5,8S rRNA (Analysis of Philogenetic Manggo (Mangifera spp.) Based On RRNA 5,8S Gene) Olivia Anafarida dan Badruzsaufari. Ziraa’Ah 45 (2016): 120–126.

Ji CY, Chen CJ, Wang XR, et al. (2017) A Report on Canker Disease of Falcataria Moluccana caused by Lasiodiplodia theobromae in China. Crop Protection 91 89–92. doi: 10.1016/j.cropro.2016.09.018.

Úrbez-Torres JR, Leavitt GM, Guerrero JC, et al. (2008) Identification and Pathogenicity of Lasiodip-lodia theobromae and Diplodia seriata, the causal Agents of Bot Canker Disease of Grapevines in Mexi-co. Plant Disease 92 (4): 519–529. doi: 10.1094/PDIS-92-4-0519.

Zhang J (2014) Lasiodiplodia theobromae in Citrus Fruit (Diplodia Stem-End Rot). Postharvest Decay Control Strateg. doi: 10.1016/B978-0-12-411552-1.00010-7

González MF, Galarza L, Valdez LL, Quizhpe GM (2023) Antifungal Activity of Metabolites from Trichoderma spp. Against Fusarium oxysporum. Bi-onatura 8 (2): 1–9. doi: 10.21931/RB/2023.08.02.7.

Damodaran T, Rajan S, Muthukumar M, et al. (2020) Biological Management of Banana Fusarium Wilt Caused by Fusarium oxysporum f. sp. cubense Tropical Race 4 Using Antagonistic Fungal Isolate CSR-T-3 (Trichoderma reesei). Frontiers in Microbiology 11 (December): 1–19. doi: 10.3389/fmicb.2020.595845.

Pandey AK, Kumar A, Samota MK, Tanti A (2022) Trichoderma reesei as an Elicitor Triggers Defense Responses in Tea Plant and Delays Gray Blight Symptoms. Pesticide Biochemistry and Physi-ology 188 (November): 105279. doi: 10.1016/j.pestbp.2022.105279.

Diversity and Efficacy Mold Rhizosphere to Control Lasiodiplodia theobromae Causing Stem-End Rot Disease on Citrus nobilis from East Kalimantan