How and Where Periglandula Fungus Interacts with Different Parts of Ipomoea asarifolia
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Species
2.2. Confirmation of Fungal Existence by Molecular Analysis
2.3. Observation of Plant-Fungal Association
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Steiner, U.; Leibner, S.; Schardl, C.L.; Leuchtmann, A.; Leistner, E. Periglandula, a new fungal genus within the Clavicipitaceae and its association with Convolvulaceae. Mycologia 2011, 103, 1133–1145. [Google Scholar] [CrossRef] [PubMed]
- Clay, K. Clavicipitaceous endophytes of grasses: Their potential as biocontrol agents. Mycol. Res. 1989, 92, 1–12. [Google Scholar] [CrossRef]
- Clay, K.; Schardl, C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat. 2002, 160, S99–S127. [Google Scholar] [CrossRef] [PubMed]
- Schardl, C.L.; Young, C.A.; Moore, N.; Krom, N.; Dupont, P.Y.; Pan, J.; Florea, S.; Webb, J.S.; Jaromczyk, J.; Jaromczyk, J.W.; et al. Genomes of plant-associated Clavicipitaceae. In Advances in Botanical Research; Francis, M.M., Ed.; Academic Press: London, UK, 2014; Volume 70, pp. 291–327. [Google Scholar]
- Porter, J.K.; Bacon, C.W.; Robbins, J.D.; Betowski, D. Ergot alkaloid identification in Clavicipitaceae systemic fungi of pasture grasses. J. Agric. Food Chem. 1981, 29, 653–657. [Google Scholar] [CrossRef]
- Torres, M.S.; Singh, A.P.; Vorsa, N.; White, J.F. An analysis of ergot alkaloids in the Clavicipitaceae (Hypocreales, Ascomycota) and ecological implications. Symbiosis 2008, 46, 11. [Google Scholar]
- Florea, S.; Panaccione, D.G.; Schardl, C.L. Ergot alkaloids of the family Clavicipitaceae. Phytopathology 2017, 107, 504–518. [Google Scholar] [CrossRef] [Green Version]
- Schardl, C.L.; Young, C.A.; Hesse, U.; Amyotte, S.G.; Andreeva, K.; Calie, P.J.; Fleetwood, D.J.; Haws, D.C.; Moore, N.; Oeser, B.; et al. Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet. 2013, 9, e1003323. [Google Scholar] [CrossRef] [Green Version]
- Cook, D.; Lee, S.T.; Panaccione, D.G.; Leadmon, C.E.; Clay, K.; Gardner, D.R. Biodiversity of Convolvulaceous species that contain ergot alkaloids, indole diterpene alkaloids, and swainsonine. Biochem. Syst. Ecol. 2019, 86, 103921. [Google Scholar] [CrossRef]
- Amor-Prats, D.; Harborne, J.B. New sources of ergoline alkaloids within the genus Ipomoea. Biochem. Syst. Ecol. 1993, 21, 455–461. [Google Scholar] [CrossRef]
- Meira, M.; Silva, E.P.D.; David, J.M.; David, J.P. Review of the genus Ipomoea: Traditional uses, chemistry and biological activities. Rev. Bras. Farmacogn. 2012, 22, 682–713. [Google Scholar] [CrossRef] [Green Version]
- Steiner, U.; Ahimsa-Müller, M.A.; Markert, A.; Kucht, S.; Groß, J.; Kauf, N.; Kuzma, M.; Zych, M.; Lamshöft, M.; Furmanowa, M.; et al. Molecular characterization of a seed transmitted clavicipitaceous fungus occurring on dicotyledoneous plants (Convolvulaceae). Planta 2006, 224, 533–544. [Google Scholar] [CrossRef] [PubMed]
- Steiner, U.; Leistner, E. Ergoline alkaloids in Convolvulaceous host plants originate from epibiotic clavicipitaceous fungi of the genus Periglandula. Fungal Ecol. 2012, 5, 316–321. [Google Scholar] [CrossRef]
- Kucht, S.; Groß, J.; Hussein, Y.; Grothe, T.; Keller, U.; Basar, S.; König, W.A.; Steiner, U.; Leistner, E. Elimination of ergoline alkaloids following treatment of Ipomoea asarifolia (Convolvulaceae) with fungicides. Planta 2004, 219, 619–625. [Google Scholar] [CrossRef]
- Ahimsa-Müller, M.A.; Markert, A.; Hellwig, S.; Knoop, V.; Steiner, U.; Drewke, C.; Leistner, E. Clavicipitaceous fungi associated with ergoline alkaloid-containing Convolvulaceae. J. Nat. Prod. 2007, 70, 1955–1960. [Google Scholar] [CrossRef] [PubMed]
- Leistner, E.; Steiner, U. The genus Periglandula and its symbiotum with morning glory plants (Convolvulaceae). The Mycota, 2nd ed.; Esser, K., Ed.; Springer: Berlin, Germany, 2018; Volume 15, pp. 131–147. [Google Scholar]
- Panaccione, D.G.; Beaulieu, W.T.; Cook, D. Bioactive alkaloids in vertically transmitted fungal endophytes. Funct. Ecol. 2014, 28, 299–314. [Google Scholar] [CrossRef] [Green Version]
- Clay, K. Hereditary symbiosis in the grass genus Danthonia. New Phytol. 1994, 126, 223–231. [Google Scholar] [CrossRef]
- Philipson, M.N.; Christey, M.C. An epiphytic/endophytic fungal associate of Danthonia spicata transmitted through the embryo sac. Bot. Gaz. 1985, 146, 70–81. [Google Scholar] [CrossRef]
- Watkinson, S.C.; Boddy, L.; Money, N. The Fungi, 3rd ed.; Academic Press: Oxford, UK, 2015; pp. 234–238. [Google Scholar]
- Staples, G.W. Convolvulaceae. In Flora of Thailand; Santisuk, T., Larsen, K., Eds.; The Forest Herbarium: Bangkok, Thailand, 2010; Volume 10, pp. 330–468. [Google Scholar]
- Brown, A.M. Detection methods and phylogenetic investigation of the morning glory associated fungal symbiont, Periglandula. Master’s Thesis, Southeastern Louisiana University, Hammond, LA, USA, 2013. [Google Scholar]
- Kaur, N.; Cooper, W.R.; Duringer, J.M.; Badillo-Vargas, I.E.; Esparza-Diaz, G.; Rashed, A.; Horton, D.R. Survival and development of potato psyllid (Hemiptera: Triozidae) on Convolvulaceae: Effects of a plant-fungus symbiosis (Periglandula). PLoS ONE 2018, 13, e0201506. [Google Scholar] [CrossRef]
- Olaranont, Y.; Stauffer, F.; Traiperm, P.; Staples, G.W. Investigation of the black dots on leaves of Stictocardia species (Convolvulaceae) using anatomical and histochemical analyses. Flora 2018, 249, 133–142. [Google Scholar] [CrossRef]
- Łaźniewska, J.; Macioszek, V.K.; Kononowicz, A.K. Plant-fungus interface: The role of surface structures in plant resistance and susceptibility to pathogenic fungi. Physiol. Mol. Plant Pathol. 2012, 78, 24–30. [Google Scholar] [CrossRef]
- Kim, K.W. Plant trichomes as microbial habitats and infection sites. Eur. J. Plant Pathol. 2019, 154, 157–169. [Google Scholar] [CrossRef]
- Markert, A.; Steffan, N.; Ploss, K.; Hellwig, S.; Steiner, U.; Drewke, C.; Li, S.M.; Boland, W.; Leistner, E. Biosynthesis and accumulation of ergoline alkaloids in a mutualistic association between Ipomoea asarifolia (Convolvulaceae) and a clavicipitalean fungus. Plant Physiol. 2008, 147, 296–305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sivapalan, A. Effects of impacting rain drops on the growth and development of powdery mildew fungi. Plant Pathol. 1993, 42, 256–263. [Google Scholar] [CrossRef]
- Inyang, E.N.; McCartney, H.A.; Oyejola, B.; Ibrahim, L.; Archer, S.A. Effect of formulation, application and rain on the persistence of the entomogenous fungus Metarhizium anisopliae on oilseed rape. Mycol. Res. 2000, 104, 653–661. [Google Scholar] [CrossRef]
- Dufault, N.S.; Isard, S.A.; Marois, J.J.; Wright, D.L. Removal of wet deposited Phakopsora pachyrhizi urediniospores from soybean leaves by subsequent rainfall. Plant Dis. 2010, 94, 1336–1340. [Google Scholar] [CrossRef] [Green Version]
- Steiner, U.; Hellwig, S.; Ahimsa-Müller, M.A.; Grundmann, N.; Li, S.M.; Drewke, C.; Leistner, E. The key role of peltate glandular trichomes in symbiota comprising clavicipitaceous fungi of the genus Periglandula and their host plants. Toxins 2015, 7, 1355–1373. [Google Scholar] [CrossRef] [Green Version]
- Rai, M.; Agarkar, G. Plant–fungal interactions: What triggers the fungi to switch among lifestyles? Crit. Rev. Microbiol. 2016, 42, 428–438. [Google Scholar] [CrossRef]
- Redman, R.S.; Dunigan, D.D.; Rodriguez, R.J. Fungal symbiosis from mutualism to parasitism: Who controls the outcome, host or invader? New Phytol. 2001, 151, 705–716. [Google Scholar] [CrossRef] [Green Version]
- Fischer, A.M. Nutrient remobilization during leaf senescence. In Senescence Processes in Plants; Gan, S., Ed.; Blackwell Publishing: New York, NY, USA, 2007; Volume 26, pp. 87–107. [Google Scholar]
- Chen, F.S.; Niklas, K.J.; Liu, Y.; Fang, X.M.; Wan, S.Z.; Wang, H. Nitrogen and phosphorus additions alter nutrient dynamics but not resorption efficiencies of Chinese fir leaves and twigs differing in age. Tree Physiol. 2015, 35, 1106–1117. [Google Scholar] [CrossRef] [Green Version]
- Marques, J.P.R.; Soares, M.K.M.; Appezzato-Da-Gloria, B. New staining technique for fungal-infected plant tissues. Turk. J. Bot. 2013, 37, 784–787. [Google Scholar]
- Huang, Y.L.; Zimmerman, N.B.; Arnold, A.E. Observations on the early establishment of foliar endophytic fungi in leaf discs and living leaves of a model woody angiosperm, Populus trichocarpa (Salicaceae). J. Fungi 2018, 4, 58. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Braga, Z.V.; dos Santos, R.F.; Amorim, L.; Appezzato-da-Glória, B. Histopathology of infection and colonisation of Elsinoë ampelina on grapevine leaves. Eur. J. Plant Pathol. 2019, 154, 1009–1019. [Google Scholar] [CrossRef]
Plant Parts | Molecular Analysis | Fluorescent Staining | Paraffin Section | SEM | |
---|---|---|---|---|---|
Young folded leaf | Adaxial surface | √ | √ (+++) | √ | √ (+++) |
Abaxial surface | - | - | - | ||
Mature leaf | Adaxial surface | √ | √ (++) | √ | √ (++) |
Abaxial surface | - | - | - | ||
Stem | - | √ (+) | - | √ (+) | |
Root | - | - | - | - | |
Flower bud and mature flower | Outer side of sepal | √ | √ (+) | - | √ (+) |
Inner side of sepal | √ (+++) | √ | √ (+++) | ||
Outer side of petal | √ (+) | √ | √ (+) | ||
Inner side of petal | - | - | - | ||
Ovules | NT | √ | NT | ||
Young seed | √ | √ (+++) | √ | √ (+++) | |
Mature seed | √ | √ (++) | NT | √ (++) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Olaranont, Y.; Stewart, A.B.; Songnuan, W.; Traiperm, P. How and Where Periglandula Fungus Interacts with Different Parts of Ipomoea asarifolia. J. Fungi 2022, 8, 823. https://doi.org/10.3390/jof8080823
Olaranont Y, Stewart AB, Songnuan W, Traiperm P. How and Where Periglandula Fungus Interacts with Different Parts of Ipomoea asarifolia. Journal of Fungi. 2022; 8(8):823. https://doi.org/10.3390/jof8080823
Chicago/Turabian StyleOlaranont, Yanisa, Alyssa B. Stewart, Wisuwat Songnuan, and Paweena Traiperm. 2022. "How and Where Periglandula Fungus Interacts with Different Parts of Ipomoea asarifolia" Journal of Fungi 8, no. 8: 823. https://doi.org/10.3390/jof8080823
APA StyleOlaranont, Y., Stewart, A. B., Songnuan, W., & Traiperm, P. (2022). How and Where Periglandula Fungus Interacts with Different Parts of Ipomoea asarifolia. Journal of Fungi, 8(8), 823. https://doi.org/10.3390/jof8080823