scholarly journals Conservation and diversity in transcriptional responses among host plants forming distinct arbuscular mycorrhizal morphotypes

2021 ◽  
Author(s):  
Takaya Tominaga ◽  
Chihiro Miura ◽  
Yuuka Sumigawa ◽  
Yukine Hirose ◽  
Katsushi Yamaguchi ◽  
...  
Keyword(s):  
Host Plants ◽  
Molecular Mechanisms ◽  
Lotus Japonicus ◽  
Arbuscular Mycorrhizal ◽  
Fungal Colonization ◽  
Intermediate Type ◽  
Transcriptional Responses ◽  
Eustoma Grandiflorum ◽  
Signal Molecule ◽  
Am Symbiosis

The morphotype of arbuscular mycorrhizal (AM) roots is distinct mostly depending on AM host species: Arum, Paris, and Intermediate types. We previously reported that gibberellin (GA) promotes the establishment of Paris-type AM symbiosis in Eustoma grandiflorum despite its negative effects on Arum-type AM symbiosis in model plants. However, the molecular mechanisms underlying the differential effects of GA on different morphotypes, including Intermediate-type AM symbiosis, remain elusive. Comparative transcriptomics revealed that several symbiosis-related genes were transcriptionally promoted upon AM fungal colonization in Lotus japonicus (Arum-type), Daucus carota (Intermediate-type), and E. grandiflorum (Paris-type). Interestingly, upon GA treatment, the fungal colonization levels and expression of symbiosis-related genes were suppressed in L. japonicus and D. carota but were promoted in E. grandiflorum. Exogenous GA transcriptionally inhibited the biosynthetic process of a host-derived signal molecule involved in AM symbiosis, strigolactone, in L. japonicus and E. grandiflorum. Additionally, disaccharides mainly metabolized in AM roots would be different between L. japonicus and D. carota/ E. grandiflorum. This study uncovered the conserved transcriptional responses during mycorrhization and diverse responses to GA in AM roots with distinct morphotypes among phylogenetically distant host plants.

scholarly journals Conservation and Diversity in Gibberellin-Mediated Transcriptional Responses Among Host Plants Forming Distinct Arbuscular Mycorrhizal Morphotypes

2021 ◽  
Vol 12 ◽  
Author(s):  
Takaya Tominaga ◽  
Chihiro Miura ◽  
Yuuka Sumigawa ◽  
Yukine Hirose ◽  
Katsushi Yamaguchi ◽  
...  
Keyword(s):  
Host Plants ◽  
Lotus Japonicus ◽  
Sugar Metabolism ◽  
Arbuscular Mycorrhizal ◽  
Fungal Colonization ◽  
Transcriptional Responses ◽  
Eustoma Grandiflorum ◽  
Transcriptional Reprogramming ◽  
Expression Of Genes ◽  
Am Symbiosis

Morphotypes of arbuscular mycorrhizal (AM) symbiosis, Arum, Paris, and Intermediate types, are mainly determined by host plant lineages. It was reported that the phytohormone gibberellin (GA) inhibits the establishment of Arum-type AM symbiosis in legume plants. In contrast, we previously reported that GA promotes the establishment of Paris-type AM symbiosis in Eustoma grandiflorum, while suppressing Arum-type AM symbiosis in a legume model plant, Lotus japonicus. This raises a hitherto unexplored possibility that GA-mediated transcriptional reprogramming during AM symbiosis is different among plant lineages as the AM morphotypes are distinct. Here, our comparative transcriptomics revealed that several symbiosis-related genes were commonly upregulated upon AM fungal colonization in L. japonicus (Arum-type), Daucus carota (Intermediate-type), and E. grandiflorum (Paris-type). Despite of the similarities, the fungal colonization levels and the expression of symbiosis-related genes were suppressed in L. japonicus and D. carota but were promoted in E. grandiflorum in the presence of GA. Moreover, exogenous GA inhibited the expression of genes involved in biosynthetic process of the pre-symbiotic signal component, strigolactone, which resulted in the reduction of its endogenous accumulation in L. japonicus and E. grandiflorum. Additionally, differential regulation of genes involved in sugar metabolism suggested that disaccharides metabolized in AM roots would be different between L. japonicus and D. carota/E. grandiflorum. Therefore, this study uncovered the conserved transcriptional responses during mycorrhization regardless of the distinct AM morphotype. Meanwhile, we also found diverse responses to GA among phylogenetically distant AM host plants.

Gibberellin Promotes Fungal Entry and Colonization during Paris-Type Arbuscular Mycorrhizal Symbiosis in Eustoma grandiflorum

2019 ◽  
Vol 61 (3) ◽  
pp. 565-575 ◽  
Author(s):  
Takaya Tominaga ◽  
Chihiro Miura ◽  
Naoya Takeda ◽  
Yuri Kanno ◽  
Yoshihiro Takemura ◽  
...  
Keyword(s):  
Arbuscular Mycorrhizal ◽  
Arbuscular Mycorrhizas ◽  
Mycorrhizal Symbiosis ◽  
Fungal Colonization ◽  
Eustoma Grandiflorum ◽  
Root Cortex ◽  
Contrasting Effect ◽  
Am Fungus ◽  
Am Symbiosis ◽  
Ga Biosynthesis

Abstract Arbuscular mycorrhizas (AMs) are divided into two types according to morphology: Arum- and Paris-type AMs. Gibberellins (GAs) mainly inhibit the establishment of Arum-type AM symbiosis in most model plants, whereas the effects of GAs on Paris-type AM symbiosis are unclear. To provide insight into the mechanism underlying this type of symbiosis, the roles of GAs were investigated in Eustoma grandiflorum when used as the host plant for Paris-type AM establishment. Eustoma grandiflorum seedlings were inoculated with the model AM fungus, Rhizophagus irregularis, and the effects of GA and the GA biosynthesis inhibitor uniconazole-P on the symbiosis were quantitatively evaluated. Exogenous GA significantly increased hyphopodium formation at the epidermis, thus leading to the promotion of fungal colonization and arbuscule formation in the root cortex. By contrast, the suppression of GA biosynthesis and signaling attenuated fungal entry to E. grandiflorum roots. Moreover, the exudates from GA-treated roots strongly induced the hyphal branching of R. irregularis. Our results show that GA has an contrasting effect on Paris-type AM symbiosis in E. grandiflorum compared with Arum-type AM symbiosis. This finding could be explained by the differential regulation of the early colonization stage, where fungal hyphae make contact with and penetrate the epidermis.

scholarly journals Strigolactone-Induced Putative Secreted Protein 1 Is Required for the Establishment of Symbiosis by the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis

2016 ◽  
Vol 29 (4) ◽  
pp. 277-286 ◽  
Author(s):  
Syusaku Tsuzuki ◽  
Yoshihiro Handa ◽  
Naoya Takeda ◽  
Masayoshi Kawaguchi
Keyword(s):  
Host Plants ◽  
Molecular Mechanisms ◽  
Mycorrhizal Fungus ◽  
Arbuscular Mycorrhizal ◽  
Rhizophagus Irregularis ◽  
Secreted Protein ◽  
Rna Seq ◽  
Am Fungus ◽  
Am Symbiosis ◽  
Reverse Genetic Approach

Arbuscular mycorrhizal (AM) symbiosis is the most widespread association between plants and fungi. To provide novel insights into the molecular mechanisms of AM symbiosis, we screened and investigated genes of the AM fungus Rhizophagus irregularis that contribute to the infection of host plants. R. irregularis genes involved in the infection were explored by RNA-sequencing (RNA-seq) analysis. One of the identified genes was then characterized by a reverse genetic approach using host-induced gene silencing (HIGS), which causes RNA interference in the fungus via the host plant. The RNA-seq analysis revealed that 19 genes are up-regulated by both treatment with strigolactone (SL) (a plant symbiotic signal) and symbiosis. Eleven of the 19 genes were predicted to encode secreted proteins and, of these, SL-induced putative secreted protein 1 (SIS1) showed the largest induction under both conditions. In hairy roots of Medicago truncatula, SIS1 expression is knocked down by HIGS, resulting in significant suppression of colonization and formation of stunted arbuscules. These results suggest that SIS1 is a putative secreted protein that is induced in a wide spatiotemporal range including both the presymbiotic and symbiotic stages and that SIS1 positively regulates colonization of host plants by R. irregularis.

scholarly journals Systemic induction of phosphatidylinositol-based signaling in leaves of arbuscular mycorrhizal rice plants

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Sonia Campo ◽  
Blanca San Segundo
Keyword(s):  
Molecular Mechanisms ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Gene Families ◽  
Transcriptional Responses ◽  
Inositol Polyphosphates ◽  
Rice Plants ◽  
Am Fungus ◽  
Am Symbiosis ◽  
Hormone Biosynthesis

Abstract Most land plants form beneficial associations with arbuscular mycorrhizal (AM) fungi which improves mineral nutrition, mainly phosphorus, in the host plant in exchange for photosynthetically fixed carbon. Most of our knowledge on the AM symbiosis derives from dicotyledonous species. We show that inoculation with the AM fungus Funneliformis mosseae stimulates growth and increases Pi content in leaves of rice plants (O. sativa, cv Loto, ssp japonica). Although rice is a host for AM fungi, the systemic transcriptional responses to AM inoculation, and molecular mechanisms underlying AM symbiosis in rice remain largely elusive. Transcriptomic analysis identified genes systemically regulated in leaves of mycorrhizal rice plants, including genes with functions associated with the biosynthesis of phospholipids and non-phosphorus lipids (up-regulated and down-regulated, respectively). A coordinated regulation of genes involved in the biosynthesis of phospholipids and inositol polyphosphates, and genes involved in hormone biosynthesis and signaling (jasmonic acid, ethylene) occurs in leaves of mycorrhizal rice. Members of gene families playing a role in phosphate starvation responses and remobilization of Pi were down-regulated in leaves of mycorrhizal rice. These results demonstrated that the AM symbiosis is accompanied by systemic transcriptional responses, which are potentially important to maintain a stable symbiotic relationship in rice plants.

scholarly journals Dual RNA-seq reveals large-scale non-conserved genotype x genotype specific genetic reprograming and molecular crosstalk in the mycorrhizal symbiosis

2018 ◽  
Author(s):  
Ivan D. Mateus ◽  
Frédéric G. Masclaux ◽  
Consolée Aletti ◽  
Edward C. Rojas ◽  
Romain Savary ◽  
...  
Keyword(s):  
Mycorrhizal Fungi ◽  
Large Scale ◽  
Molecular Mechanisms ◽  
Arbuscular Mycorrhizal ◽  
Mycorrhizal Symbiosis ◽  
Rna Seq ◽  
Plant Host ◽  
Transcriptional Responses ◽  
Plant Genes ◽  
Fungal Genetic

AbstractArbuscular mycorrhizal fungi (AMF) impact plant growth and are a major driver of plant diversity and productivity. We quantified the contribution of intra-specific genetic variability in cassava (Manihot esculenta) and Rhizophagus irregularis to gene reprogramming in symbioses using dual RNA-sequencing. A large number of cassava genes exhibited altered transcriptional responses to the fungus but transcription of most of these plant genes (72%) responded in a different direction or magnitude depending on the plant genotype. Two AMF isolates displayed large differences in their transcription, but the direction and magnitude of the transcriptional responses for a large number of these genes was also strongly influenced by the genotype of the plant host. This indicates that unlike the highly conserved plant genes necessary for the symbiosis establishment, plant and fungal gene transcriptional responses are not conserved and are greatly influenced by plant and fungal genetic differences, even at the within-species level. The transcriptional variability detected allowed us to identify an extensive gene network showing the interplay in plant-fungal reprogramming in the symbiosis. Key genes illustrated that the two organisms jointly program their cytoskeleton organisation during growth of the fungus inside roots. Our study reveals that plant and fungal genetic variation plays a strong role in shaping the genetic reprograming in response to symbiosis, indicating considerable genotype x genotype interactions in the mycorrhizal symbiosis. Such variation needs to be considered in order to understand the molecular mechanisms between AMF and their plant hosts in natural communities.

scholarly journals Integrative Analysis of the Wheat PHT1 Gene Family Reveals A Novel Member Involved in Arbuscular Mycorrhizal Phosphate Transport and Immunity

Cells ◽  
2019 ◽  
Vol 8 (5) ◽  
pp. 490 ◽  
Author(s):  
Yi Zhang ◽  
Lizong Hu ◽  
Deshui Yu ◽  
Kedong Xu ◽  
Ju Zhang ◽  
...  
Keyword(s):  
Arbuscular Mycorrhizal ◽  
Phosphate Transport ◽  
P Uptake ◽  
Mode Analysis ◽  
Fungal Colonization ◽  
Wheat Roots ◽  
Transcription Analysis ◽  
P Deficiency ◽  
Am Symbiosis ◽  
Inducible Genes

Phosphorus (P) deficiency is one of the main growth-limiting factors for plants. However, arbuscular mycorrhizal (AM) symbiosis can significantly promote P uptake. Generally, PHT1 transporters play key roles in plants’ P uptake, and thus, PHT1 genes have been investigated in some plants, but the regulation and functions of these genes in wheat (TaPHT1) during AM symbiosis have not been studied in depth. Therefore, a comprehensive analysis of TaPHT1 genes was performed, including sequence, phylogeny, cis-elements, expression, subcellular localization and functions, to elucidate their roles in AM-associated phosphate transport and immunity. In total, 35 TaPHT1s were identified in the latest high-quality bread wheat genome, 34 of which were unevenly distributed on 13 chromosomes, and divided into five groups. Sequence analysis indicated that there are 11 types of motif architectures and five types of exon-intron structures in the TaPHT1 family. Duplication mode analysis indicated that the TaPHT1 family has expanded mainly through segmental and tandem duplication events, and that all duplicated gene pairs have been under purifying selection. Transcription analysis of the 35 TaPHT1s revealed that not only known the mycorrhizal-specific genes TaPht-myc, TaPT15-4B (TaPT11) and TaPT19-4D (TaPT10), but also four novel mycorrhizal-specific/inducible genes (TaPT3-2D, TaPT11-4A, TaPT29-6A, and TaPT31-7A) are highly up-regulated in AM wheat roots. Furthermore, the mycorrhizal-specific/inducible genes are significantly induced in wheat roots at different stages of infection by colonizing fungi. Transient Agrobacterium tumefaciens-mediated transformation expression in onion epidermal cells showed that TaPT29-6A is a membrane-localized protein. In contrast to other AM-specific/inducible PHT1 genes, TaPT29-6A is apparently required for the symbiotic and direct Pi pathway. TaPT29-6A-silenced lines exhibited reduced levels of AM fungal colonization and arbuscules, but increased susceptibility to biotrophic, hemi-biotrophic and necrotrophic pathogens. In conclusion, TaPT29-6A was not only essential for the AM symbiosis, but also played vital roles in immunity.

scholarly journals Elucidating the Mechanisms Underlying Enhanced Drought Tolerance in Plants Mediated by Arbuscular Mycorrhizal Fungi

2021 ◽  
Vol 12 ◽  
Author(s):  
Shen Cheng ◽  
Ying-Ning Zou ◽  
Kamil Kuča ◽  
Abeer Hashem ◽  
Elsayed Fathi Abd_Allah ◽  
...  
Keyword(s):  
Drought Stress ◽  
Drought Tolerance ◽  
Mycorrhizal Fungi ◽  
Host Plants ◽  
Molecular Mechanisms ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Host Cells ◽  
Future Research ◽  
Symbiotic Association

Plants are often subjected to various environmental stresses during their life cycle, among which drought stress is perhaps the most significant abiotic stress limiting plant growth and development. Arbuscular mycorrhizal (AM) fungi, a group of beneficial soil fungi, can enhance the adaptability and tolerance of their host plants to drought stress after infecting plant roots and establishing a symbiotic association with their host plant. Therefore, AM fungi represent an eco-friendly strategy in sustainable agricultural systems. There is still a need, however, to better understand the complex mechanisms underlying AM fungi-mediated enhancement of plant drought tolerance to ensure their effective use. AM fungi establish well-developed, extraradical hyphae on root surfaces, and function in water absorption and the uptake and transfer of nutrients into host cells. Thus, they participate in the physiology of host plants through the function of specific genes encoded in their genome. AM fungi also modulate morphological adaptations and various physiological processes in host plants, that help to mitigate drought-induced injury and enhance drought tolerance. Several AM-specific host genes have been identified and reported to be responsible for conferring enhanced drought tolerance. This review provides an overview of the effect of drought stress on the diversity and activity of AM fungi, the symbiotic relationship that exists between AM fungi and host plants under drought stress conditions, elucidates the morphological, physiological, and molecular mechanisms underlying AM fungi-mediated enhanced drought tolerance in plants, and provides an outlook for future research.

Novel Insights into Host Receptors and Receptor-mediated Signaling that Regulate Arbuscular Mycorrhizal Symbiosis

2020 ◽  
Author(s):  
Fahad Nasir ◽  
Ali Bahadur ◽  
Xiaolong Lin ◽  
Yingzhi Gao ◽  
Chunjie Tian
Keyword(s):  
Host Plant ◽  
Host Plants ◽  
Agronomic Traits ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Land Plant ◽  
Physical Contact ◽  
Mycorrhizal Symbiosis ◽  
Downstream Signaling ◽  
Am Symbiosis

Abstract More than 80% of land plant species benefit from symbiotic partnerships with arbuscular mycorrhizal (AM) fungi that assist in nutrient acquisition and enhance the ability of host plants to adapt to environmental constraints. Host-generated plasma membrane-residing receptor-like kinases and the α/β-hydrolases, e.g. DWARF14-LIKE (D14L), a putative karrikin receptor, are used to detect the presence of AM fungi prior to physical contact between the host and fungus. Detection induces the activation of symbiosis-related transcriptional programming, enabling the successful establishment of AM symbiosis. In order to prevent hyper-colonization and to maintain a mutually beneficial association, the host plants precisely monitor and control AM symbiosis during the post-symbiotic stage via different molecular strategies. While previous studies have elucidated how host plant receptors and receptor-mediated signaling regulate AM symbiosis, the molecular details underlying these processes remain poorly understood. The recent identification of a rice (Oryza sativa) CHITIN-ELICITOR RECEPTOR-KINASE 1 (OsCERK1) interaction partner MYC FACTOR RECEPTOR 1 (OsMYR1), as well as new insights into D14L-receptor- and SUPER NUMERIC NODULES 1 (SUNN1) receptor-mediated signaling have improved our understanding of how host plant receptors and their corresponding signaling regulate AM symbiosis. The present review summarizes these and other current findings that have increased our limited understanding of receptor-mediated signaling mechanisms involved in the regulation of AM symbiosis. The identified receptors and/or their downstream signaling components could potentially be used to engineer economically-important crops with improved agronomic traits by conferring the ability to control the colonization of AM fungi in a precise manner.

scholarly journals Investigation of Indigenous Arbuscular Mycorrhizal Performance Using a Lotus japonicus Mycorrhizal Mutant

Plants ◽  
2020 ◽  
Vol 9 (5) ◽  
pp. 658
Author(s):  
Taisuke Teranishi ◽  
Yoshihro Kobae
Keyword(s):  
Plant Growth ◽  
Arbuscular Mycorrhiza ◽  
Host Plants ◽  
Lotus Japonicus ◽  
Soil Management ◽  
Arbuscular Mycorrhizal ◽  
Mineral Nutrients ◽  
Wild Type ◽  
Arbuscular Mycorrhiza Fungi ◽  
Mycorrhizal Roots

Most plants are usually colonized with arbuscular mycorrhiza fungi (AMF) in the fields. AMF absorb mineral nutrients, especially phosphate, from the soil and transfer them to the host plants. Inoculation with exotic AMF is thought to be effective when indigenous AMF performance is low; however, there is no method for evaluating the performance of indigenous AMF. In this study, we developed a method to investigate the performance of indigenous AMF in promoting plant growth. As Lotus japonicus mutant (str) that are unable to form functional mycorrhizal roots were considered to be symbiosis negative for indigenous mycorrhizal performance, we examined the growth ratios of wild-type and str mycorrhizal mutant using 24 soils. Each soil had its own unique indigenous mycorrhizal performance, which was not directly related to the colonization level of indigenous AMF or soil phosphate level. The low indigenous mycorrhizal performance could not be compensated by the inoculation of exotic AMF. Importantly, indigenous mycorrhizal performance was never negative; however, the inoculation of exotic AMF into the same soil led to both positive and negative performances. These results suggest that indigenous mycorrhizal performance is affected by soil management history and is basically harmless to the plant.

scholarly journals Mycorrhizal symbiosis alleviates plant drought stress within and across plant generations via plasticity

2020 ◽  
Author(s):  
Javier Puy ◽  
Carlos Perez Carmona ◽  
Inga Hiiesalu ◽  
Maarja Opik ◽  
Mari Moora ◽  
...  
Keyword(s):  
Drought Stress ◽  
Phenotypic Plasticity ◽  
Water Availability ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Mycorrhizal Symbiosis ◽  
Fungal Colonization ◽  
Transgenerational Effects ◽  
Two Generations ◽  
Am Symbiosis

Phenotypic plasticity is essential for organisms to adapt to local ecological conditions. Little is known about how mutualistic interactions, such as arbuscular mycorrhizal (AM) symbiosis, mediate plant phenotypic plasticity and to what extent this plasticity may be heritable (i.e. transgenerational effects). We tested for plant plasticity within- and across-generations in response to AM symbiosis and varying water availability in a full factorial experiment over two generations, using the perennial apomictic herb Taraxacum brevicorniculatum. We examined changes in phenotype, performance, and AM fungal colonization of the offspring throughout plant development. AM symbiosis and water availability triggered phenotypic changes during the life cycle of plants. Additionally, both triggered adaptive transgenerational effects, especially detectable during the juvenile stage. Drought stress and absence of AM fungi caused concordant plant phenotypic modifications towards a stress-coping phenotype within- and across-generations. AM fungal colonization of offspring was also affected by the parental environment. AM symbiosis can trigger transgenerational effects, including changes in functional traits related to resource-use acquisition and AM fungal colonization of the offspring, in turn affecting the biotic interaction. Thus, transgenerational effects of mycorrhizal symbiosis are not limited to plant fitness, but also improve plants ability to cope with environmental stress.

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