Functional Insights into the Roles of Hormones in the Dendrobium officinale-Tulasnella sp. Germinated Seed Symbiotic Association

Dendrobium is one of the largest genera in the Orchidaceae, and D. officinale is used in traditional medicine, particularly in China. D. officinale seeds are minute and contain limited energy reserves, and colonization by a compatible fungus is essential for germination under natural conditions. When the orchid mycorrhizal fungi (OMF) initiates symbiotic interactions with germination-driven orchid seeds, phytohormones from the orchid or the fungus play key roles, but the details of the possible biochemical pathways are still poorly understood. In the present study, we established a symbiotic system between D. officinale and Tulasnella sp. for seed germination. RNA-Seq was used to construct libraries of symbiotic-germinated seeds (DoTc), asymbiotic-germinated seeds (Do), and free-living OMF (Tc) to investigate the expression profiles of biosynthesis and metabolism pathway genes for three classes of endogenous hormones: JA (jasmonic acid), ABA (abscisic acid) and SLs (strigolactones), in D. officinale seeds and OMF under symbiotic and asymbiotic conditions. Low concentrations of endogenous JA, ABA, or SLs were detected in the D. officinale-Tulasnella symbiont compared with the asymbiotic tissues. Gene annotation results suggest that the expression of DEGs (differentially expressed genes) related to JA and ABA biosynthesis from D. officinale were down-regulated, while most of the key DEGs related to SL biosynthesis from D. officinale were up-regulated in the symbiotic germinated seeds compared with the asymbiotic germinated seeds. Moreover, in the OMF, we found a significantly up-regulated differential expression of the JA and ABA biosynthesis-related genes in the symbiotic interaction, with the opposite expression trends to those found in Dendrobium. This indicates that Dendrobium seed symbiotic germination may be stimulated by the apparent involvement of the OMF in the production of hormones, and relatively low concentrations of endogenous JA, ABA, or SLs might be maintained to promote the growth of the D. officinale-Tulasnella symbiotic protocorm-like body. These results will increase our understanding of the possible roles played by endogenous hormones in the regulation of the orchid-fungus symbiosis.

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Biochemical and transcriptomic analyses of the symbiotic interaction between Cremastra appendiculata and the mycorrhizal fungus Coprinellus disseminatus

BMC Plant Biology ◽

10.1186/s12870-021-03388-6 ◽

2022 ◽

Vol 22 (1) ◽

Author(s):

Yanyan Gao ◽

Jun Ji ◽

Yujin Zhang ◽

Ningxian Yang ◽

Mingsheng Zhang

Keyword(s):

Gene Annotation ◽

Lignin Content ◽

Water Status ◽

Mycorrhizal Fungus ◽

Symbiotic Interaction ◽

Symbiotic Germination ◽

Cremastra Appendiculata ◽

Rate Of Decline ◽

Different Levels ◽

Β Carotene

Abstract Background Cremastra appendiculata is a rare terrestrial orchid with a high market value as an ornamental and medicinal plant. However, the species depends entirely on fungi for seed germination under natural conditions. In a previous study, we have successfully isolated and identified the mycorrhizal fungus Coprinellus disseminatus which was able to induce the germination of C. appendiculata seeds. We then speculated that C. disseminatus may do so by breaking the testa imposed dormancy of the seeds. In this study, biochemical and transcriptomic analyses were used to characterize the germination of C. appendiculata seeds, collected at different stages of germination, as affected by C. disseminatus. Results The lignocellulose in the seeds coat of C. appendiculata was degraded by the mycorrhizal fungus resulting in facilitated absorption of water. The rate of decline in lignin content was 67 and 73% at 6 and 12 days after sowing, respectively. The water content increased from 13 to 90% during symbiosis. A total of 15,382 genes showing significantly different levels of expression (log2 FPKM≥2.0, Qvalue≤0.05) were successfully identified among all libraries, where the highest number of DEGs was shared between 6 days versus 0 day after symbiotic germination. Gene annotation results suggested that 15 key genes related water-status, such as DHN gene family and Xero 1 were down-regulated. The genes zeaxanthin epoxidase ZEP, 9-cis-epoxycarotenoid dioxygenase NCED3 and β-carotene hydroxylase involved in the biosynthesis of abscisic acid (ABA) were significantly down-regulated in 6 days as compared to 0 day after symbiotic germination. Conclusions This work demonstrates that mycorrhizal fungus C. disseminatus can stimulate C. appendiculata seeds germination through a mechanism of breaking the testa imposed dormancy and inducing water absorption of the embryo.

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Phosphatidic acid produced by phospholipase D is required for hyphal cell-cell fusion and fungal-plant symbiosis

10.1101/849232 ◽

2019 ◽

Author(s):

Berit Hassing ◽

Carla J. Eaton ◽

David Winter ◽

Kimberly A. Green ◽

Ulrike Brandt ◽

...

Keyword(s):

Phosphatidic Acid ◽

Filamentous Fungi ◽

Cell Fusion ◽

Phospholipase D ◽

Axenic Culture ◽

Symbiotic Association ◽

Symbiotic Interaction ◽

Hyphal Morphogenesis ◽

The Impact ◽

Cell Cell

SummaryAlthough lipid signaling has been shown to serve crucial roles in mammals and plants, little is known about this process in filamentous fungi. Here we analyse the contribution of phospholipase D (PLD) and its product phosphatidic acid (PA) in hyphal morphogenesis and growth of Epichloë festucae and Neurospora crassa, and in the establishment of a symbiotic interaction between E. festucae and Lolium perenne. Growth of E. festucae and N. crassa PLD deletion strains in axenic culture, and for E. festucae in association with L. perenne, were analysed by light-, confocal- and electron microscopy. Changes in PA distribution were analysed in E. festucae using a PA biosensor and the impact of these changes on endocytic recycling and superoxide production investigated. We found that E. festucae PldB and the N. crassa ortholog, PLA-7, are required for polarized growth, cell fusion and ascospore development, whereas PldA/PLA-8 are dispensable for these functions. Exogenous addition of PA rescues the cell-fusion phenotype in E. festucae. PldB is also crucial for E. festucae to establish a symbiotic association with L. perenne. This study identifies a new component of the cell-cell communication and cell fusion signaling network that controls hyphal morphogenesis and growth in filamentous fungi.

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The Medicago truncatula N5 Gene Encoding a Root-Specific Lipid Transfer Protein Is Required for the Symbiotic Interaction with Sinorhizobium meliloti

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-22-12-1577 ◽

2009 ◽

Vol 22 (12) ◽

pp. 1577-1587 ◽

Cited By ~ 33

Author(s):

Youry Pii ◽

Alessandra Astegno ◽

Elisa Peroni ◽

Massimo Zaccardelli ◽

Tiziana Pandolfini ◽

...

Keyword(s):

Medicago Truncatula ◽

Sinorhizobium Meliloti ◽

Lipid Transfer Protein ◽

Symbiotic Association ◽

Lipid Transfer ◽

Symbiotic Interaction ◽

Transgenic Roots ◽

Transfer Protein ◽

Small Proteins

The Medicago truncatula N5 gene is induced in roots after Sinorhizobium meliloti infection and it codes for a putative lipid transfer protein (LTP), a family of plant small proteins capable of binding and transferring lipids between membranes in vitro. Various biological roles for plant LTP in vivo have been proposed, including defense against pathogens and modulation of plant development. The aim of this study was to shed light on the role of MtN5 in the symbiotic interaction between M. truncatula and S. meliloti. MtN5 cDNA was cloned and the mature MtN5 protein expressed in Escherichia coli. The lipid binding capacity and antimicrobial activity of the recombinant MtN5 protein were tested in vitro. MtN5 showed the capacity to bind lysophospholipids and to inhibit M. truncatula pathogens and symbiont growth in vitro. Furthermore, MtN5 was upregulated in roots after infection with either the fungal pathogen Fusarium semitectum or the symbiont S. meliloti. Upon S. meliloti infection, MtN5 was induced starting from 1 day after inoculation (dpi). It reached the highest concentration at 3 dpi and it was localized in the mature nodules. MtN5-silenced roots were impaired in nodulation, showing a 50% of reduction in the number of nodules compared with control roots. On the other hand, transgenic roots overexpressing MtN5 developed threefold more nodules with respect to control roots. Here, we demonstrate that MtN5 possesses biochemical features typical of LTP and that it is required for the successful symbiotic association between M. truncatula and S. meliloti.

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The role of strigolactones in host specificity ofOrobancheandPhelipancheseed germination

Seed Science Research ◽

10.1017/s0960258510000371 ◽

2010 ◽

Vol 21 (1) ◽

pp. 55-61 ◽

Cited By ~ 58

Author(s):

Mónica Fernández-Aparicio ◽

Koichi Yoneyama ◽

Diego Rubiales

Keyword(s):

Seed Germination ◽

Host Specificity ◽

Mycorrhizal Fungi ◽

Arbuscular Mycorrhizal ◽

Parasitic Plants ◽

Parasitic Weed ◽

Low Concentrations ◽

Weedy Species ◽

Germination Requirements

AbstractStrigolactones are apocarotenoids regulating shoot branching. They are also known to be exuded by plant roots at very low concentrations, stimulating hyphal branching of arbuscular mycorrhizal fungi and germination of root parasitic weed seeds. We show that strigolactones play a major role in host specificity ofOrobancheandPhelipanche(the broomrapes) seed germination. This observation confirms that host-derived germination stimulants are an important component determining the host specificity of these parasitic plants. Weedy broomrape species were less specialized in germination requirements than the non-weedy species except forO. cumanaandO. foetidavar.broteri. Similar results were obtained with the root exudates. Some species, such asP. aegyptiacaandO. minor, showed a broad spectrum of host specificity in terms of seed germination, which was stimulated by exudates from the majority of species tested, whereas others, such asO. cumana,O. hederaeandO. densiflora, were highly specific. Some species, such asO. minor,P. aegyptiacaandP. nana, were responsive to the three strigolactones studied, whereas others were induced by only one of them, or did not respond to them at all. The synthetic strigolactone analogue GR24, generally used as a standard for germination tests, was not effective on someOrobancheandPhelipanchespecies. Seeds of some species that did not respond to GR24 were induced to germinate in the presence of fabacyl acetate or strigol, confirming the role of strigolactones in host specificity.

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Beneficial soil-borne bacteria and fungi: a promising way to improve plant nitrogen acquisition

Journal of Experimental Botany ◽

10.1093/jxb/eraa112 ◽

2020 ◽

Vol 71 (15) ◽

pp. 4469-4479 ◽

Cited By ~ 5

Author(s):

Alia Dellagi ◽

Isabelle Quillere ◽

Bertrand Hirel

Keyword(s):

Mycorrhizal Fungi ◽

Current Knowledge ◽

Essential Element ◽

Symbiotic Association ◽

Terrestrial Plants ◽

Plant Nitrogen ◽

N Nutrition ◽

Symbiotic Associations ◽

N Fertilizers ◽

Bacteria And Fungi

Abstract Nitrogen (N) is an essential element for plant productivity, thus, it is abundantly applied to the soil in the form of organic or chemical fertilizers that have negative impacts on the environment. Exploiting the potential of beneficial microbes and identifying crop genotypes that can capitalize on symbiotic associations may be possible ways to significantly reduce the use of N fertilizers. The best-known example of symbiotic association that can reduce the use of N fertilizers is the N2-fixing rhizobial bacteria and legumes. Bacterial taxa other than rhizobial species can develop associative symbiotic interactions with plants and also fix N. These include bacteria of the genera Azospirillum, Azotobacter, and Bacillus, some of which are commercialized as bio-inoculants. Arbuscular mycorrhizal fungi are other microorganisms that can develop symbiotic associations with most terrestrial plants, favoring access to nutrients in a larger soil volume through their extraradical mycelium. Using combinations of different beneficial microbial species is a promising strategy to boost plant N acquisition and foster a synergistic beneficial effect between symbiotic microorganisms. Complex biological mechanisms including molecular, metabolic, and physiological processes dictate the establishment and efficiency of such multipartite symbiotic associations. In this review, we present an overview of the current knowledge and future prospects regarding plant N nutrition improvement through the use of beneficial bacteria and fungi associated with plants, individually or in combination.

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Symbiotic and Asymbiotic Germination of Dendrobium officinale (Orchidaceae) Respond Differently to Exogenous Gibberellins

International Journal of Molecular Sciences ◽

10.3390/ijms21176104 ◽

2020 ◽

Vol 21 (17) ◽

pp. 6104 ◽

Cited By ~ 2

Author(s):

Juan Chen ◽

Bo Yan ◽

Yanjing Tang ◽

Yongmei Xing ◽

Yang Li ◽

...

Keyword(s):

Seed Germination ◽

Mycorrhizal Fungi ◽

Calcium Binding ◽

Germination Rate ◽

Dendrobium Officinale ◽

Fungal Colonization ◽

Fungal Mycelium ◽

High Concentration ◽

Symbiotic Germination ◽

Asymbiotic Germination

Seeds of almost all orchids depend on mycorrhizal fungi to induce their germination in the wild. The regulation of this symbiotic germination of orchid seeds involves complex crosstalk interactions between mycorrhizal establishment and the germination process. The aim of this study was to investigate the effect of gibberellins (GAs) on the symbiotic germination of Dendrobium officinale seeds and its functioning in the mutualistic interaction between orchid species and their mycobionts. To do this, we used liquid chromatograph-mass spectrometer to quantify endogenous hormones across different development stages between symbiotic and asymbiotic germination of D. officinale, as well as real-time quantitative PCR to investigate gene expression levels during seed germination under the different treatment concentrations of exogenous gibberellic acids (GA3). Our results showed that the level of endogenous GA3 was not significantly different between the asymbiotic and symbiotic germination groups, but the ratio of GA3 and abscisic acids (ABA) was significantly higher during symbiotic germination than asymbiotic germination. Exogenous GA3 treatment showed that a high concentration of GA3 could inhibit fungal colonization in the embryo cell and decrease the seed germination rate, but did not significantly affect asymbiotic germination or the growth of the free-living fungal mycelium. The expression of genes involved in the common symbiotic pathway (e.g., calcium-binding protein and calcium-dependent protein kinase) responded to the changed concentrations of exogenous GA3. Taken together, our results demonstrate that GA3 is probably a key signal molecule for crosstalk between the seed germination pathway and mycorrhiza symbiosis during the orchid seed symbiotic germination.

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Unraveling Arbuscular Mycorrhiza-Induced Changes in Plant Primary and Secondary Metabolome

Metabolites ◽

10.3390/metabo10080335 ◽

2020 ◽

Vol 10 (8) ◽

pp. 335 ◽

Cited By ~ 1

Author(s):

Sukhmanpreet Kaur ◽

Vidya Suseela

Keyword(s):

Secondary Metabolites ◽

Mycorrhizal Fungi ◽

Tricarboxylic Acid Cycle ◽

Abiotic Stress Tolerance ◽

Plant Performance ◽

Growth And Yield ◽

Primary Metabolism ◽

Symbiotic Association ◽

Phytochemical Content ◽

Primary And Secondary Metabolites

Arbuscular mycorrhizal fungi (AMF) is among the most ubiquitous plant mutualists that enhance plant growth and yield by facilitating the uptake of phosphorus and water. The countless interactions that occur in the rhizosphere between plants and its AMF symbionts are mediated through the plant and fungal metabolites that ensure partner recognition, colonization, and establishment of the symbiotic association. The colonization and establishment of AMF reprogram the metabolic pathways of plants, resulting in changes in the primary and secondary metabolites, which is the focus of this review. During initial colonization, plant–AMF interaction is facilitated through the regulation of signaling and carotenoid pathways. After the establishment, the AMF symbiotic association influences the primary metabolism of the plant, thus facilitating the sharing of photosynthates with the AMF. The carbon supply to AMF leads to the transport of a significant amount of sugars to the roots, and also alters the tricarboxylic acid cycle. Apart from the nutrient exchange, the AMF imparts abiotic stress tolerance in host plants by increasing the abundance of several primary metabolites. Although AMF initially suppresses the defense response of the host, it later primes the host for better defense against biotic and abiotic stresses by reprogramming the biosynthesis of secondary metabolites. Additionally, the influence of AMF on signaling pathways translates to enhanced phytochemical content through the upregulation of the phenylpropanoid pathway, which improves the quality of the plant products. These phytometabolome changes induced by plant–AMF interaction depends on the identity of both plant and AMF species, which could contribute to the differential outcome of this symbiotic association. A better understanding of the phytochemical landscape shaped by plant–AMF interactions would enable us to harness this symbiotic association to enhance plant performance, particularly under non-optimal growing conditions.

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Identification of Immune Regulatory Genes in Apis mellifera through Caffeine Treatment

Insects ◽

10.3390/insects11080516 ◽

2020 ◽

Vol 11 (8) ◽

pp. 516 ◽

Cited By ~ 1

Author(s):

Yun-Heng Lu ◽

Carol-P Wu ◽

Cheng-Kang Tang ◽

Yu-Hsien Lin ◽

Houda Ouns Maaroufi ◽

...

Keyword(s):

Expression Profiles ◽

Insect Immunity ◽

Protective Measure ◽

Valuable Insight ◽

Deformed Wing Virus ◽

Naturally Occurring ◽

Copy Numbers ◽

Expression Of Genes ◽

Low Concentrations ◽

Pharmacologically Active

Plants and pollinators are mutually beneficial: plants provide nectar as a food source and in return their pollen is disseminated by pollinators such as honeybees. Some plants secrete chemicals to deter herbivores as a protective measure, among which is caffeine, a naturally occurring, bitter tasting, and pharmacologically active secondary compound. It can be found in low concentrations in the nectars of some plants and as such, when pollinators consume nectar, they also take in small amounts of caffeine. Whilst caffeine has been indicated as an antioxidant in both mammals and insects, the effect on insect immunity is unclear. In the present study, honeybees were treated with caffeine and the expression profiles of genes involved in immune responses were measured to evaluate the influence of caffeine on immunity. In addition, honeybees were infected with deformed wing virus (DWV) to study how caffeine affects their response against pathogens. Our results showed that caffeine can increase the expression of genes involved in immunity and reduce virus copy numbers, indicating that it has the potential to help honeybees fight against viral infection. The present study provides a valuable insight into the mechanism by which honeybees react to biotic stress and how caffeine can serve as a positive contributor, thus having a potential application in beekeeping.

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Symbiotic association between golden berry (Physalis peruviana) and arbuscular mycorrhizal fungi in heavy metal-contaminated soil

Journal of Plant Protection Research ◽

10.1515/jppr-2017-0024 ◽

2017 ◽

Vol 57 (2) ◽

pp. 173-184 ◽

Cited By ~ 5

Author(s):

Marieta Hristozkova ◽

Maria Geneva ◽

Ira Stancheva ◽

Ivan Iliev ◽

Concepción Azcón-Aguilar

Keyword(s):

Fatty Acids ◽

Heavy Metal ◽

Arbuscular Mycorrhizal Fungi ◽

Mycorrhizal Fungi ◽

Arbuscular Mycorrhizal ◽

Protein Accumulation ◽

Symbiotic Association ◽

Tropical Fruit ◽

Physalis Peruviana ◽

Mycorrhizal Association

AbstractPhysalis peruvianais one of the most promising tropical fruit plants because of its rapid growth, high yield, and nutritional quality. This study was designed to investigate plant development under heavy metal contamination (Cd, Pb) and responsiveness to arbuscular mycorrhizal fungi (AMF) colonization byRhizophagus clarumandClaroideoglomus claroideum. The antioxidant capacity, total lipid content and fatty acid profile in fruits, accumulation of Cd and Pb in different plant parts, plant dry biomass, and mycorrhizal colonization were determined. As a result of inoculation, a considerable reduction in Cd and Pb in the fruits was observed, compared with non-inoculated plants. The fruit number and dry weight increased in plants associated withC. claroideum.These plants also showed higher acid phosphatase activity, root protein accumulation and glomalin production. The type of antioxidant defense was AMF strain-dependent. Antioxidant activity and H2O2neutralization were enzymatic rather than non-enzymatic processes in the fruits ofC. claroideumplants compared with those forming an association withR. clarum. Mycorrhizal establishment changed the composition and concentration of fruits’ fatty acids. The ratio of unsaturated fatty acids was increased. With respect to the accumulation of bioactive compounds in golden berry the present findings are important for obtaining the optimum benefits of mycorrhizal association under unfavorable conditions.

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