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.

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.

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 Target of rapamycin, PvTOR, is a key regulator of arbuscule development during mycorrhizal symbiosis in Phaseolus

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Manoj-Kumar Arthikala ◽  
Kalpana Nanjareddy ◽  
Lourdes Blanco ◽  
Xóchitl Alvarado-Affantranger ◽  
Miguel Lara
Keyword(s):  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Target Of Rapamycin ◽  
Mycorrhizal Symbiosis ◽  
Energy Status ◽  
Symbiotic Associations ◽  
Expression Of Genes ◽  
Fungal Symbiosis ◽  
Am Fungus ◽  
Am Symbiosis

AbstractTarget of rapamycin (TOR) is a conserved central growth regulator in eukaryotes that has a key role in maintaining cellular nutrient and energy status. Arbuscular mycorrhizal (AM) fungi are mutualistic symbionts that assist the plant in increasing nutrient absorption from the rhizosphere. However, the role of legume TOR in AM fungal symbiosis development has not been investigated. In this study, we examined the function of legume TOR in the development and formation of AM fungal symbiosis. RNA-interference-mediated knockdown of TOR transcripts in common bean (Phaseolus vulgaris) hairy roots notably suppressed AM fungus-induced lateral root formation by altering the expression of root meristem regulatory genes, i.e., UPB1, RGFs, and sulfur assimilation and S-phase genes. Mycorrhized PvTOR-knockdown roots had significantly more extraradical hyphae and hyphopodia than the control (empty vector) roots. Strong promoter activity of PvTOR was observed at the site of hyphal penetration and colonization. Colonization along the root length was affected in mycorrhized PvTOR-knockdown roots and the arbuscules were stunted. Furthermore, the expression of genes induced by AM symbiosis such as SWEET1, VPY, VAMP713, and STR was repressed under mycorrhized conditions in PvTOR-knockdown roots. Based on these observations, we conclude that PvTOR is a key player in regulating arbuscule development during AM symbiosis in P. vulgaris. These results provide insight into legume TOR as a potential regulatory factor influencing the symbiotic associations of P. vulgaris and other legumes.

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.

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.

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 A Phosphate-Dependent Requirement for Transcription Factors IPD3 and IPD3L During Arbuscular Mycorrhizal Symbiosis in Medicago truncatula

2019 ◽  
Vol 32 (10) ◽  
pp. 1277-1290
Author(s):  
Penelope L. Lindsay ◽  
Brandon N. Williams ◽  
Allyson MacLean ◽  
Maria J. Harrison
Keyword(s):  
Gene Expression ◽  
Signaling Pathway ◽  
Medicago Truncatula ◽  
Lotus Japonicus ◽  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Mycorrhizal Symbiosis ◽  
Wild Type ◽  
Symbiotic Gene ◽  
Am Symbiosis

During arbuscular mycorrhizal (AM) symbiosis, activation of a symbiosis signaling pathway induces gene expression necessary for accommodation of AM fungi. Here, we focus on pathway components Medicago truncatula INTERACTING PROTEIN OF DOES NOT MAKE INFECTIONS 3 (IPD3) and IPD3 LIKE (IPD3L), which are potential orthologs of Lotus japonicus CYCLOPS, a transcriptional regulator essential for AM symbiosis. In the double mutant ipd3 ipd3l, hyphal entry through the epidermis and overall colonization levels are reduced relative to the wild type but fully developed arbuscules are present in the cortex. In comparison with the wild type, colonization of ipd3 ipd3l is acutely sensitive to higher phosphate levels in the growth medium, with a disproportionate decrease in epidermal penetration, overall colonization, and symbiotic gene expression. When constitutively expressed in ipd3 ipd3l, an autoactive DOES NOT MAKE INFECTIONS 3 induces the expression of transcriptional regulators REDUCED ARBUSCULAR MYCORRHIZA 1 and REQUIRED for ARBUSCULE DEVELOPMENT 1, providing a possible avenue for arbuscule development in the absence of IPD3 and IPD3L. An increased sensitivity of ipd3 ipd3l to GA3 suggests an involvement of DELLA. The data reveal partial redundancy in the symbiosis signaling pathway, which may ensure robust signaling in low-phosphorus environments, while IPD3 and IPD3L maintain signaling in higher-phosphorus environments. The latter may buffer the pathway from short-term variation in phosphorus levels encountered by roots during growth in heterogeneous soil environments.

scholarly journals Medicago SPX1 and SPX3 regulate phosphate homeostasis, mycorrhizal colonization, and arbuscule degradation

2021 ◽  
Author(s):  
Peng Wang ◽  
Roxane Snijders ◽  
Wouter Kohlen ◽  
Jieyu Liu ◽  
Ton Bisseling ◽  
...  
Keyword(s):  
Arbuscular Mycorrhizal ◽  
Am Fungi ◽  
Mineral Nutrients ◽  
Fungal Colonization ◽  
Phosphate Homeostasis ◽  
Pi Starvation ◽  
Biosynthesis Gene ◽  
Am Symbiosis ◽  
Phosphate Response ◽  
Inner Cortex

Abstract To acquire sufficient mineral nutrients such as phosphate (Pi) from the soil, most plants engage in symbiosis with arbuscular mycorrhizal (AM) fungi. Attracted by plant-secreted strigolactones (SLs), the fungi colonize the roots and form highly branched hyphal structures called arbuscules inside inner cortex cells. The host plant must control the different steps of this interaction to maintain its symbiotic nature. However, how plants sense the amount of Pi obtained from the fungus, and how this determines the arbuscule lifespan, are far from understood. Here, we show that Medicago truncatula SPX-domain containing proteins SPX1 and SPX3 regulate root Pi starvation responses, in part by interacting with PHOSPHATE RESPONSE REGULATOR2, as well as fungal colonization and arbuscule degradation. SPX1 and SPX3 are induced upon Pi starvation but become more restricted to arbuscule-containing cells upon the establishment of symbiosis. This induction in arbuscule-containing cells is associated with the presence of cis-regulatory AW-boxes and transcriptional regulation by the WRINKLED1-like transcription factor WRI5a. Under Pi-limiting conditions, SPX1 and SPX3 facilitate the expression of the SL biosynthesis gene DWARF27, which could help explain the increased fungal branching in response to root exudates. Later, in arbuscule-containing cells, SPX1 and SPX3 redundantly control arbuscule degradation. Thus, SPX proteins play important roles as phosphate sensors to maintain a beneficial AM symbiosis.

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