An Overview of Stress-Tolerant Promoting Endophytic Fungal Isolates from Hiyung Chilli Grown in South Kalimantan: Endophytic Fungi of Hiyung Chilli Peppers

Witiyasti Imaningsih; Nuraeni  Ekowati; Salamiah; Nuniek Ina Ratnaningtyas; Loekas Soesanto

doi:10.11594/jtls.13.01.18

Authors

Witiyasti Imaningsih Universitas Lambung Mangkurat
Nuraeni Ekowati Biology Faculty, Universitas Jenderal Soedirman, 53122, ,Purwokerto-Central Java, Indonesia https://orcid.org/0000-0002-5927-0967
Salamiah Plant Protection Study Program, Faculty of Agriculture, Universitas Lambung Mangkurat, 70714, Banjabaru-South Kalimantan, Indonesia https://orcid.org/0000-0003-4171-1231
Nuniek Ina Ratnaningtyas Biology Faculty, Universitas Jenderal Soedirman, 53122, ,Purwokerto-Central Java, Indonesia https://orcid.org/0000-0002-7841-1999
Loekas Soesanto Faculty of Agriculture, Universitas Jenderal Soedirman, 53122, Purwokerto-Central Java, Indonesia https://orcid.org/0000-0002-6501-4177

DOI:

https://doi.org/10.11594/jtls.13.01.18

Keywords:

Anti-pathogenic fungi, auxin, capsaicin, indonesian chili, south Kalimantan

Abstract

Endophytic fungi are a unique class of microorganisms that lives in plant tissues. These fungi could spread from roots to shoots and interact with nearly all plants in a symbiotic, mutualistic, or commensal manner. Endophytic fungi are believed to exert several roles related to plant growth, including the ability to tolerate stress, especially in Hiyung chilli plants. This plant is widely cultivated in Indonesia and is a well-known host for endophytic fungi. The Hiyung chilli is a popular variety grown in the South Kalimantan Province, which receives national recognition and is geographically certified by the Indonesian government. This wetland-cultivated chilli plant has a uniquely high capsaicin content and long fruit shelf life compared to other varieties. Although endophytic fungal isolates are prevalently found on chilli plants, their potential to influence the growth of their host remains to be proven beyond a doubt. This review emphasizes the sparse reports on the potential of these antagonistic fungi in protecting chilli plants against other pathogens by producing auxin/Indole-3-Acetic Acid (IAA) and capsaicin. The study hypothesised that the antagonistic abilities of these endophytic fungi against other fungal pathogens are related to their IAA- and capsaicin production that synergistically increase the chili plants' threshold against biotic and abiotic stress.

References

Hamdani, Salawati U, Nuryadin R (2017) Daya Saing Agribisnis Dan Potensi Pengembangan Cabe Hiyung Di Kabupaten Tapin, Kalimantan Selatan. Prosiding Seminar Nasional Lahan Basah Jilid 1 156–163.

Sutomo, Rahmawati A, Rizki MI (2017) Standarisasi Buah Cabe Rawit Hiyung ( Capsicum frutescens L .) Asal Tapin Kalimantan Selatan. 2 (September): 245–253. doi: 10.36387/jiis.v2i2.121.

Wahdah R, Rahmawati Y, Nafarin Y et al. (2016) Deskripsi Cabai Rawit Varietas Hiyung. Lampiran Surat Keputusan Menteri Pertanian Republik Indonesia Nomor : 031/Kpts/SR.120/D.2.7/4/2016 Deskripsi.

Pramudyani L, Sabran M, Noor A (2019) Agronomic Performance and Nutrition Content of Hiyung as Local Variety of Cayenne Pepper [Capsicum frutescens] at Dry Land and Swamp Land of South Kalimantan Province. Buletin Plasma Nutfah 25 (1): 43. doi: 10.21082/blpn.v25n1.2019.p43-52.

Direktorat Merek dan Indikasi Geografis KEMENKUMHAM (2019) Berita Resmi Indikasi Geografis Seri-A no.No. 17/IG/X/A/2019. Direktorat Merek dan Indikasi Geografis. Direktorat Jenderal Kekayaan Intelektual. KEMENKUMHAMRI.

Budi IS, Mariana M (2016) Controlling Anthracnose Disease of Locally Chili in Marginal Wetland using Endophytic Indigenous Microbes and Kalakai (Stenochlaena palustris) Leaf Extract. Journal of Wetlands Environmental Management 4 (1): 28–34. doi: 10.20527/jwem.v4i1.51.

Imaningsih W, Mariana, Junaedi AB, Rasyidah (2021) Antifungal activities of the combination of ulin wood liquid smoke and hiyung cayenne pepper root endophyte fungi against Colletothricum capsici. Agrivita 43 (1): 69–78. doi: 10.17503/agrivita.v1i1.2458.

Herrera-Parra E, Cristóbal-Alejo J, Ramos-Zapata JA (2017) Trichoderma strains as growth promoters in Capsicum annuum and as biocontrol agents in Meloidogyne incognita. Chilean Journal of Agricultural Research 77 (4): 318–324. doi: 10.4067/S0718-58392017000400318.

Handayani D, Fifendy M, Yesni V (2018) Isolation of Phosphate Solubilizing Endophytic Fungi From Rice Plant Root. Bioscience 2 (1): 93. doi: 10.24036/020182110043-0-00.

Sati SC, Pant P (2019) Two Root Endophytic Aquatic Hyphomycetes Campylospora parvula and Tetracladium setigerum as Plant Growth Promoters. Asian Journal of Agricultural Research 14 (1): 28–33. doi: 10.3923/ajar.2020.28.33.

Khan MS, Gao J, Munir I et al. (2021) Characterization of Endophytic Fungi, Acremonium sp., from Lilium davidii and Analysis of Its Antifungal and Plant Growth-Promoting Effects. BioMed Research International 2021 1–14. doi: 10.1155/2021/9930210.

Singh N, Singh A, Dahiya P (2021) Plant Growth-Promoting Endophytic Fungi from Different Habitats and Their Potential Applications in Agriculture. pp 69–87.

Rigobelo EC, Baron NC (2021) Endophytic fungi: a tool for plant growth promotion and sustainable agriculture. Mycology 13 (1): 39-55. doi: 10.1080/21501203.2021.1945699.

Syamsia S, Idhan A, Firmansyah AP et al. (2021) Combination on endophytic fungal as the Plant Growth-Promoting Fungi (PGPF) on cucumber (Cucumis sativus). Biodiversitas Journal of Biological Diversity 22 (3): 1194–1202. doi: 10.13057/biodiv/d220315.

Imaningsih W, Rahayu ND, Hakim SS (2021) Endophytes and Rhizosphere Fungi from Galam (Melaleuca cajuputi Powell.) which has the Potential to Produce Indole Acetic Acid (IAA). Journal of Tropical Biodiversity and Biotechnology 6 (2): 61594. doi: 10.22146/jtbb.61594.

Devari S, Jaglan S, Kumar M et al. (2014) Capsaicin production by Alternaria alternata, an endophytic fungus from Capsicum annum; LC-ESI-MS/MS analysis. Phytochemistry 98: 183–189. doi: 10.1016/j.phytochem.2013.12.001.

Hutauruk ICP, Hasanuddin, Pinem MI (2020) Ability test of endophytic fungi to suppress the development of anthracnose disease (Colletotrichum capsici) in chili plants (Capsicum annum) in the Karo Highland. IOP Conf Ser Earth Environ Sci. doi: 10.1088/1755-1315/454/1/012185.

Hernawati H, Wiyono S, Santoso S (2011) Leaf endophytic fungi of chili (Capsicum annuum) and their role in the protection against Aphis gossypii (Homoptera: Aphididae). Biodiversitas Journal of Biological Diversity 12 (4): 187–191. doi: 10.13057/biodiv/d120401.

Lestari SM, Hidayat SH, Widodo W (2018) Determination of Endophytic Fungi as Induce Resistance Agent of Chilli Pepper Against Pepper Yellow Leaf Curl Disease. AGRIVITA Journal of Agricultural Science 40 (2): 249–256. doi: 10.17503/agrivita.v40i2.989.

Paul NC, Deng JX, Sang H-K et al. (2012) Distribution and Antifungal Activity of Endophytic Fungi in Different Growth Stages of Chili Pepper (Capsicum annuum L.) in Korea. The Plant Pathology Journal 28 (1): 10–19. doi: 10.5423/PPJ.OA.07.2011.0126.

Rajamanikyam M, Vadlapudi V, Amanchy R, Upadhyayula SM (2017) Endophytic Fungi as Novel Resources of natural Therapeutics. Arch Biol Technol v Arch Biol Technol v 606060 (December): 1–26. doi: 10.1590/1678-4324-2017160542.

Abhijeet Singh YM (2014) Understanding the Biodiversity and Biological Applications of Endophytic Fungi: A Review. J Microb Biochem Technol. doi: 10.4172/1948-5948.S8-004.

Abhijeet Singh YM (2014) Understanding the Biodiversity and Biological Applications of Endophytic Fungi: A Review. J Microb Biochem Technol. doi: 10.4172/1948-5948.s8-004

Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: Diversity and functional roles: Tansley review. New Phytologist 182 (2): 314–330. doi: 10.1111/j.1469-8137.2009.02773.x.

Christian N, Herre EA, Clay K (2019) Foliar endophytic fungi alter patterns of nitrogen uptake and distribution in Theobroma cacao. New Phytologist 222 (3): 1573–1583. doi: 10.1111/nph.15693.

Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J. doi: 10.1155/2014/250693

Deshmukh S, Hückelhoven R, Schäfer P et al. (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proceedings of the National Academy of Sciences 103 (49): 18450–18457. doi: 10.1073/pnas.0605697103.

Lata R, Chowdhury S, Gond SK, White JF (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Letters in Applied Microbiology 66 (4): 268–276. doi: 10.1111/lam.12855.

Hiruma K, Gerlach N, Sacristán S et al. (2016) Root Endophyte Colletotrichum tofieldiae Confers Plant Fitness Benefits that Are Phosphate Status Dependent. Cell 165 (2): 464–474. doi: 10.1016/j.cell.2016.02.028.

Paradiso R, Arena C, De Micco V et al. (2017) Changes in leaf anatomical traits enhanced photosynthetic activity of soybean grown in hydroponics with plant growth-promoting microorganisms. Frontiers in Plant Science 8 (May): 1–13. doi: 10.3389/fpls.2017.00674.

Suebrasri T, Harada H, Jogloy S et al. (2020) Auxin-producing fungal endophytes promote growth of sunchoke. Rhizosphere 16 (100271): 100271. doi: 10.1016/j.rhisph.2020.100271.

Hayati A, Hardarani N (2019) Karakteristik Lahan dan Budidaya Cabai Rawit Hiyung: Informasi Dasar untuk Peningkatan Produksi Cabai Rawit Hiyung di Lahan Rawa Lebak. Prosding Seminar Nasional Lingkungan Lahan Basah 4 (1): 57–59.

Mathivanan S (2021) Abiotic Stress-Induced Molecular and Physiological Changes and Adaptive Mechanisms in Plants. In: Abiotic Stress Plants. IntechOpen, pp 137–144.

Manganyi MC, Ateba CN (2020) Untapped potentials of endophytic fungi: A review of novel bioactive compounds with biological applications. Microorganisms 8 (12): 1–25. doi: 10.3390/microorganisms8121934.

Huda N, Imaningsih W, Hakim SS (2019) Uji Antagonisme Kapang Endofit Tanaman Galam (Melaleuca cajuputi) terhadap Colletotrichum truncatum. Jurnal Mikologi Indonesia 3 (2): 59. doi: 10.46638/jmi.v3i2.62.

Imaningsih W, Adventaria D, Mariana, Junaidi AB (2022) Inhibitory Effect Of Ulinwood Liquid Smoke and Gogo Rice Endophytic Fungi Against Pathogen Pyricularia oryzae. Biotropia 29 (1): 23–32. doi: 10.11598/btb.2022.29.1.1568.

Bae H, Roberts DP, Lim H-S et al. (2011) Endophytic Trichoderma Isolates from Tropical Environments Delay Disease Onset and Induce Resistance Against Phytophthora capsici in Hot Pepper Using Multiple Mechanisms. Molecular Plant-Microbe Interactions® 24 (3): 336–351. doi: 10.1094/MPMI-09-10-0221.

Nurzannah S, Lisnawita L, Bakti D (2014) Potensi Jamur Endofit Asal Cabai Sebagai Agens Hayati Untuk Mengendalikan Layu Fusarium (Fusarium Oxysporum) Pada Cabai Dan Interaksinya. Jurnal Agroekoteknologi Universitas Sumatera Utara 2 (3): 100407. doi: 10.32734/jaet.v2i3.7543.

Lubna, Asaf S, Hamayun M et al. (2018) Aspergillus Niger CSR3 regulates plant endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic acid. Journal of Plant Interactions 13 (1): 100–111. doi: 10.1080/17429145.2018.1436199.

Herrera-Parra E, Cristóbal-Alejo J, Ramos-Zapata JA Trichoderma strains as growth promoters in Capsicum annuum and as biocontrol agents in Meloidogyne incognita. Chil J Agric Res. doi: 10.4067/S0718-58392017000400318.

Egamberdieva D, Wirth SJ, Alqarawi AA et al. (2017) Phytohormones and Beneficial Microbes: Essential Components for Plants to Balance Stress and Fitness. Frontiers in Microbiology 8 (OCT): 1–14. doi: 10.3389/fmicb.2017.02104.

Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annual Review of Plant Biology 61 (May): 49–64. doi: 10.1146/annurev-arplant-042809-112308.

Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Advances 29 (2): 248–258. doi: 10.1016/j.biotechadv.2010.12.001.

Glick BR, Todorovic B, Czarny J et al. (2007) Promotion of Plant Growth by Bacterial ACC Deaminase. Critical Reviews in Plant Sciences 26 (5–6): 227–242. doi: 10.1080/07352680701572966.

Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: Molecular plant-rhizobacteria interactions. Plant, Cell and Environment 26 (2): 189–199. doi: 10.1046/j.1365-3040.2003.00956.x.

Noriler SA, Savi DC, Aluizio R et al. (2018) Bioprospecting and Structure of Fungal Endophyte Communities Found in the Brazilian Biomes, Pantanal, and Cerrado. Frontiers in Microbiology 9 (JUL): 1–14. doi: 10.3389/fmicb.2018.01526.

Turbat A, Rakk D, Vigneshwari A et al. (2020) Characterization of the Plant Growth-Promoting Activities of Endophytic Fungi Isolated from Sophora flavescens. Microorganisms 8 (5): 683. doi: 10.3390/microorganisms8050683.

Alarcón MV, Salguero J, Lloret PG (2019) Auxin modulated initiation of lateral roots is linked to pericycle cell length in Maize. Frontiers in Plant Science 10 (January): 1–10. doi: 10.3389/fpls.2019.00011.

Singh A, Singh DK, Kharwar RN et al. (2021) Fungal Endophytes as Efficient Sources of Plant-Derived Bioactive Compounds and Their Prospective Applications in Natural Product Drug Discovery: Insights, Avenues, and Challenges. Microorganisms 9 (1): 197. doi: 10.3390/microorganisms9010197.

Al Othman ZA, Ahmed YBH, Habila MA, Ghafar AA (2011) Determination of capsaicin and dihydrocapsaicin in Capsicum fruit samples using high performance liquid chromatography. Molecules 16 (10): 8919–8929. doi: 10.3390/molecules16108919.

Tewksbury JJ, Reagan KM, Machnicki NJ et al. (2008) Evolutionary ecology of pungency in wild chilies. Proceedings of the National Academy of Sciences of the United States of America 105 (33): 11808–11811. doi: 10.1073/pnas.0802691105.

Barchenger DW, Bosland PW (2016) Exogenous applications of capsaicin inhibits seed germination of Capsicum annuum. Scientia Horticulturae 203: 29–31. doi: 10.1016/j.scienta.2016.03.009.

Luna-ruiz JDJ, Nabhan GP, Aguilar-meléndez A (2018) Shifts in Plant Chemical Defenses of Chile Pepper (Capsicum annuum L.) Due to Domestication in Mesoamerica. doi: 10.3389/fevo.2018.00048

Chabaane Y, Marques Arce C, Glauser G, Benrey B (2022) Altered capsaicin levels in domesticated chili pepper varieties affect the interaction between a generalist herbivore and its ectoparasitoid. Journal of Pest Science 95 (2): 735–747. doi: 10.1007/s10340-021-01399-8.

Haak DC, McGinnis LA, Levey DJ, Tewksbury JJ (2012) Why are not all chilies hot? A trade-off limits pungency. Proceedings of the Royal Society B: Biological Sciences 279 (1735): 2012–2017. doi: 10.1098/rspb.2011.2091.

Adams CA, Zimmerman K, Fenstermacher K et al. (2020) Fungal seed pathogens of wild chili peppers possess multiple mechanisms to tolerate capsaicinoids. Appl Environ Microbiol. doi: 10.1128/AEM.01697-19

Mahmudah N, Badruzsaufari B (2020) Analisis Kekerabatan Fenetik Cabai Hiyung Dengan Beberapa Kultivar Cabai Rawit. Ziraa'ah Majalah Ilmiah Pertanian 45 (2): 135. doi: 10.31602/zmip.v45i2.2997.

Menteri Pertanian Republik Indonesia (2011) Deskripsi Cabai rawit Varietas Nirmala.

Dey P, Datta D, Saha D et al. (2019) Plant-Endophyte Interaction and Its Application to Abiotic Stress Management of Crop Plants. International Journal of Current Microbiology and Applied Sciences 8 (07): 2708–2716. doi: 10.20546/ijcmas.2019.807.332.

Ali S, Charles TC, Glick BR (2017) Functional Importance of the Plant Microbiome. Funct Importance Plant Microbiome Implic Agric For Bioenergy. doi: 10.1007/978-3-319-65897-1.

Kumara PM, Shweta S, M, M V et al. (2014) Advances in Endophytic Research, Advances i. Adv Endophytic Res. doi: 10.1007/978-81-322-1575-2

Bian M, Zhou M, Sun D, Li C (2013) Molecular approaches unravel the mechanism of acid soil tolerance in plants. Crop Journal 1 (2): 91–104. doi: 10.1016/j.cj.2013.08.002.

Mengistu AA (2020) Endophytes: Colonization, Behaviour, and Their Role in Defense Mechanism. International Journal of Microbiology 2020 1–8. doi: 10.1155/2020/6927219.

Chitarra W, Hamayun M, Khan AW et al. (2021) Fungal Endophyte: An Interactive Endosymbiont With the Capability of Modulating Host Physiology in Myriad Ways. Front Plant Sci 12: 701800. doi: 10.3389/fpls.2021.701800.

Popelka P, Jevinová P, Šmejkal K, Roba P (2017) Determination of Capsaicin Content and Pungency Level of Different Fresh and Dried Chilli Peppers. Folia Veterinaria 61 (2): 11–16. doi: 10.1515/fv-2017-0012.

Orellana-Escobedo L, Garcia-Amezquita LE, Olivas GI et al. (2013) Capsaicinoids content and proximate composition of Mexican chili peppers (Capsicum spp.) cultivated in the State of Chihuahua. CyTA - Journal of Food 11 (2): 179–184. doi: 10.1080/19476337.2012.716082.

Waite MS, Aubin AJ, Corporation W (2008) A Modular HPLC System for routine Analysis of Capsaicin from Hot Sauces. Waters Corporation 1 (1): 1–5.