Phosphorus Starvation- and Zinc Excess-Induced Astragalus sinicus AsZIP2 Zinc Transporter Is Suppressed by Arbuscular Mycorrhizal Symbiosis

Zinc (Zn) is one of the most essential micronutrients for plant growth and metabolism, but Zn excess can impair many basic metabolic processes in plant cells. In agriculture, crops often experience low phosphate (Pi) and high Zn double nutrient stresses because of inordinate agro-industrial activities, while the dual benefit of arbuscular mycorrhizal (AM) fungi protects plants from experiencing both deficient and toxic nutrient stresses. Although crosstalk between Pi and Zn nutrients in plants have been extensively studied at the physiological level, the molecular basis of how Pi starvation triggers Zn over-accumulation in plants and how AM plants coordinately modulate the Pi and Zn nutrient homeostasis remains to be elucidated. Here, we report that a novel AsZIP2 gene, a Chinese milk vetch (Astragalus sinicus) member of the ZIP gene family, participates in the interaction between Pi and Zn nutrient homeostasis in plants. Phylogenetic analysis revealed that this AsZIP2 protein was closely related to the orthologous Medicago MtZIP2 and Arabidopsis AtZIP2 transporters. Gene expression analysis indicated that AsZIP2 was highly induced in roots by Pi starvation or Zn excess yet attenuated by arbuscular mycorrhization in a Pi-dependent manner. Subcellular localization and heterologous expression experiments further showed that AsZIP2 encoded a functional plasma membrane-localized transporter that mediated Zn uptake in yeast. Moreover, overexpression of AsZIP2 in A. sinicus resulted in the over-accumulation of Zn concentration in roots at low Pi or excessive Zn concentrations, whereas AsZIP2 silencing lines displayed an even more reduced Zn concentration than control lines under such conditions. Our results reveal that the AsZIP2 transporter functioned in Zn over-accumulation in roots during Pi starvation or high Zn supply but was repressed by AM symbiosis in a Pi-dependent manner. These findings also provide new insights into the AsZIP2 gene acting in the regulation of Zn homeostasis in mycorrhizal plants through Pi signal.

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Phytohormones Regulate the Development of Arbuscular Mycorrhizal Symbiosis

International Journal of Molecular Sciences ◽

10.3390/ijms19103146 ◽

2018 ◽

Vol 19 (10) ◽

pp. 3146 ◽

Cited By ~ 19

Author(s):

Dehua Liao ◽

Shuangshuang Wang ◽

Miaomiao Cui ◽

Jinhui Liu ◽

Aiqun Chen ◽

...

Keyword(s):

Early Recognition ◽

Fungal Growth ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Mycorrhizal Symbiosis ◽

Dependent Manner ◽

Terrestrial Plants ◽

Root Cells ◽

Della Proteins ◽

Am Symbiosis

Most terrestrial plants are able to form a root symbiosis with arbuscular mycorrhizal (AM) fungi for enhancing the assimilation of mineral nutrients. AM fungi are obligate symbionts that depend on host plants as their sole carbon source. Development of an AM association requires a continuous signal exchange between the two symbionts, which triggers coordinated differentiation of both partners, to enable their interaction within the root cells. The control of the AM symbiosis involves a finely-tuned process, and an increasing number of studies have pointed to a pivotal role of several phytohormones, such as strigolactones (SLs), gibberellic acids (GAs), and auxin, in the modulation of AM symbiosis, through the early recognition of events up to the final arbuscular formation. SLs are involved in the presymbiotic growth of the fungus, while auxin is required for both the early steps of fungal growth and the differentiation of arbuscules. GAs modulate arbuscule formation in a dose-dependent manner, via DELLA proteins, a group of GRAS transcription factors that negatively control the GA signaling. Here, we summarize the recent findings on the roles of these plant hormones in AM symbiosis, and also explore the current understanding of how the DELLA proteins act as central regulators to coordinate plant hormone signaling, to regulate the AM symbiosis.

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Expression Pattern Suggests a Role of MiR399 in the Regulation of the Cellular Response to Local Pi Increase During Arbuscular Mycorrhizal Symbiosis

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-23-7-0915 ◽

2010 ◽

Vol 23 (7) ◽

pp. 915-926 ◽

Cited By ~ 101

Author(s):

Anja Branscheid ◽

Daniela Sieh ◽

Bikram Datt Pant ◽

Patrick May ◽

Emanuel A. Devers ◽

...

Keyword(s):

Cellular Response ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Mycorrhizal Symbiosis ◽

Pi Homeostasis ◽

Pi Starvation ◽

Mycorrhizal Roots ◽

Am Symbiosis ◽

Pi Stress

Many plants improve their phosphate (Pi) availability by forming mutualistic associations with arbuscular mycorrhizal (AM) fungi. Pi-repleted plants are much less colonized by AM fungi than Pi-depleted plants. This indicates a link between plant Pi signaling and AM development. MicroRNAs (miR) of the 399 family are systemic Pi-starvation signals important for maintenance of Pi homeostasis in Arabidopsis thaliana and might also qualify as signals regulating AM development in response to Pi availability. MiR399 could either represent the systemic low-Pi signal promoting or required for AM formation or they could act as counter players of systemic Pi-availability signals that suppress AM symbiosis. To test either of these assumptions, we analyzed the miR399 family in the AM-capable plant model Medicago truncatula and could experimentally confirm 10 novel MIR399 genes in this species. Pi-depleted plants showed increased expression of mature miR399 and multiple pri-miR399, and unexpectedly, levels of five of the 15 pri-miR399 species were higher in leaves of mycorrhizal plants than in leaves of nonmycorrhizal plants. Compared with nonmycorrhizal Pi-depleted roots, mycorrhizal roots of Pi-depleted M. truncatula and tobacco plants had increased Pi contents due to symbiotic Pi uptake but displayed higher mature miR399 levels. Expression levels of MtPho2 remained low and PHO2-dependent Pi-stress marker transcript levels remained high in these mycorrhizal roots. Hence, an AM symbiosis-related signal appears to increase miR399 expression and decrease PHO2 activity. MiR399 overexpression in tobacco suggested that miR399 alone is not sufficient to improve mycorrhizal colonization supporting the assumption that, in mycorrhizal roots, increased miR399 are necessary to keep the MtPho2 expression and activity low, which would otherwise increase in response to symbiotic Pi uptake.

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Arbuscular mycorrhizal symbiosis facilitates apricot seedling (Prunus sibirica L.) growth and photosynthesis in northwest China

International Journal of Coal Science & Technology ◽

10.1007/s40789-021-00408-6 ◽

2021 ◽

Author(s):

Yinli Bi ◽

Linlin Xie ◽

Zhigang Wang ◽

Kun Wang ◽

Wenwen Liu ◽

...

Keyword(s):

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Northwest China ◽

Shaanxi Province ◽

Mycorrhizal Symbiosis ◽

Seedling Physiology ◽

Grassland Ecosystems ◽

Time Period ◽

Seedling Biomass ◽

Experimental Treatments

AbstractArbuscular mycorrhizal (AM) fungi can successfully enhance photosynthesis (Pn) and plants growth in agricultural or grassland ecosystems. However, how the symbionts affect species restoration in sunlight-intensive areas remains largely unexplored. Therefore, this study’s objective was to assess the effect of AM fungi on apricot seedling physiology, within a specific time period, in northwest China. In 2010, an experimental field was established in Shaanxi Province, northwest China. The experimental treatments included two AM fungi inoculation levels (0 or 100 g of AM fungal inoculum per seedling), three shade levels (1900, 1100, and 550 µmol m−2 s−1), and three ages (1, 3, and 5 years) of transplantation. We examined growth, Pn, and morphological indicators of apricot (Prunus sibirica L.) seedling performances in 2011, 2013, and 2015. The colonization rate in mycorrhizal seedlings with similar amounts of shade is higher than the corresponding controls. The mycorrhizal seedling biomass is significantly higher than the corresponding non-mycorrhizal seedling biomass. Generally, Pn, stomatal conductance (Gs), transpiration rate (Tr), and water use efficiency are also significantly higher in the mycorrhizal seedlings. Moreover, mycorrhizal seedlings with light shade (LS) have the highest Pn. WUE is increased in non-mycorrhizal seedlings because of the reduction in Tr, while Tr is increased in mycorrhizal seedlings with shade. There is a significant increase in the N, P, and K fractions detected in roots compared with shoots. This means that LS had apparent benefits for mycorrhizal seedlings. Our results also indicate that AM fungi, combined with LS, exert a positive effect on apricot behavior.

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Extraction of short chain chitooligosaccharides from fungal biomass and their use as promoters of arbuscular mycorrhizal symbiosis

Scientific Reports ◽

10.1038/s41598-021-83299-6 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Andrea Crosino ◽

Elisa Moscato ◽

Marco Blangetti ◽

Gennaro Carotenuto ◽

Federica Spina ◽

...

Keyword(s):

Fungal Biomass ◽

Large Scale ◽

Low Cost ◽

Trichoderma Viride ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Production Costs ◽

Short Chain ◽

Mycorrhizal Symbiosis ◽

Major Interest

AbstractShort chain chitooligosaccharides (COs) are chitin derivative molecules involved in plant-fungus signaling during arbuscular mycorrhizal (AM) interactions. In host plants, COs activate a symbiotic signalling pathway that regulates AM-related gene expression. Furthermore, exogenous CO application was shown to promote AM establishment, with a major interest for agricultural applications of AM fungi as biofertilizers. Currently, the main source of commercial COs is from the shrimp processing industry, but purification costs and environmental concerns limit the convenience of this approach. In an attempt to find a low cost and low impact alternative, this work aimed to isolate, characterize and test the bioactivity of COs from selected strains of phylogenetically distant filamentous fungi: Pleurotus ostreatus, Cunninghamella bertholletiae and Trichoderma viride. Our optimized protocol successfully isolated short chain COs from lyophilized fungal biomass. Fungal COs were more acetylated and displayed a higher biological activity compared to shrimp-derived COs, a feature that—alongside low production costs—opens promising perspectives for the large scale use of COs in agriculture.

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

Scientific Reports ◽

10.1038/s41598-021-90288-2 ◽

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.

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Integrating physiological, community, and evolutionary perspectives on the arbuscular mycorrhizal symbiosis

Botany ◽

10.1139/cjb-2013-0182 ◽

2014 ◽

Vol 92 (4) ◽

pp. 241-251 ◽

Cited By ~ 33

Author(s):

Ylva Lekberg ◽

Roger T. Koide

Keyword(s):

Evolutionary Biology ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Partner Choice ◽

Mycorrhizal Symbiosis ◽

Physiological Processes ◽

Resource Transfers ◽

Am Symbiosis ◽

Controlled Environments ◽

Natural Settings

Our knowledge of arbuscular mycorrhizal (AM) function is largely based on results from short-term studies in controlled environments. While these have provided many important insights into the potential effects of the symbiosis on the two symbionts and their communities, they may have also inadvertently led to faulty assumptions about the function of the symbiosis in natural settings. Here we highlight the consequences of failing to consider the AM symbiosis from the perspectives of community ecology and evolutionary biology. Also, we argue that by distinguishing between physiological and evolutionary viewpoints, we may be able to resolve controversies regarding the mutualistic vs. parasitic nature of the symbiosis. Further, while most AM research has emphasized resource transfers, primarily phosphate and carbohydrate, our perceptions of parasitism, cheating, bet-hedging, and partner choice would most likely change if we considered other services. Finally, to gain a fuller understanding of the role of the AM symbiosis in nature, we need to better integrate physiological processes of plants and their AM fungi with their naturally occurring temporal and spatial patterns. It is our hope that this article will generate some fruitful discussions and make a contribution toward this end.

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Differential Response of Mycorrhizal Plants to Tomato bushy stunt virus and Tomato mosaic virus Infection

Microorganisms ◽

10.3390/microorganisms8122038 ◽

2020 ◽

Vol 8 (12) ◽

pp. 2038

Author(s):

Neda Khoshkhatti ◽

Omid Eini ◽

Davoud Koolivand ◽

Antreas Pogiatzis ◽

John N. Klironomos ◽

...

Keyword(s):

Mosaic Virus ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Tomato Bushy Stunt Virus ◽

Uninfected Control ◽

Tomato Mosaic Virus ◽

Mycorrhizal Symbiosis ◽

Pr Genes ◽

Tomato Plants ◽

Virus Accumulation

Tomato bushy stunt virus (TBSV) and Tomato mosaic virus (ToMV) are important economic pathogens in tomato fields. Rhizoglomus irregulare is a species of arbuscular mycorrhizal (AM) fungus that provides nutrients to host plants. To understand the effect of R. irregulare on the infection by TBSV/ToMV in tomato plants, in a completely randomized design, five treatments, including uninfected control plants without AM fungi (C), uninfected control plants with AM fungi (M) TBSV/ToMV-infected plants without AM fungi (V), TBSV/ToMV-infected plants before mycorrhiza (VM) inoculation, and inoculated plants with mycorrhiza before TBSV/ToMV infection (MV), were studied. Factors including viral RNA accumulation and expression of Pathogenesis Related proteins (PR) coding genes including PR1, PR2, and PR3 in the young leaves were measured. For TBSV, a lower level of virus accumulation and a higher expression of PR genes in MV plants were observed compared to V and VM plants. In contrast, for ToMV, a higher level of virus accumulation and a lower expression of PR genes in MV plants were observed as compared to V and VM plants. These results indicated that mycorrhizal symbiosis reduces or increases the viral accumulation possibly via the regulation of PR genes in tomato plants.

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Arbuscular Mycorrhizal Symbiosis Affects Plant Immunity to Viral Infection and Accumulation

Viruses ◽

10.3390/v11060534 ◽

2019 ◽

Vol 11 (6) ◽

pp. 534 ◽

Cited By ~ 8

Author(s):

Zhipeng Hao ◽

Wei Xie ◽

Baodong Chen

Keyword(s):

Viral Infection ◽

Plant Immunity ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Plant Viruses ◽

Limiting Factors ◽

Systemic Resistance ◽

Mycorrhizal Symbiosis ◽

Complex Nature ◽

Terrestrial Plants

Arbuscular mycorrhizal (AM) fungi, as root symbionts of most terrestrial plants, improve plant growth and fitness. In addition to the improved plant nutritional status, the physiological changes that trigger metabolic changes in the root via AM fungi can also increase the host ability to overcome biotic and abiotic stresses. Plant viruses are one of the important limiting factors for the commercial cultivation of various crops. The effect of AM fungi on viral infection is variable, and considerable attention is focused on shoot virus infection. This review provides an overview of the potential of AM fungi as bioprotection agents against viral diseases and emphasizes the complex nature of plant–fungus–virus interactions. Several mechanisms, including modulated plant tolerance, manipulation of induced systemic resistance (ISR), and altered vector pressure are involved in such interactions. We propose that using “omics” tools will provide detailed insights into the complex mechanisms underlying mycorrhizal-mediated plant immunity.

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Photosynthetic performance and stevioside concentration are improved by the arbuscular mycorrhizal symbiosis in Stevia rebaudiana under different phosphate concentrations

PeerJ ◽

10.7717/peerj.10173 ◽

2020 ◽

Vol 8 ◽

pp. e10173

Author(s):

Luis G. Sarmiento-López ◽

Melina López-Meyer ◽

Gabriela Sepúlveda-Jiménez ◽

Luis Cárdenas ◽

Mario Rodríguez-Monroy

Keyword(s):

Stevia Rebaudiana ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

P Uptake ◽

Photosynthetic Performance ◽

Phosphate Concentration ◽

Mycorrhizal Symbiosis ◽

Steviol Glycosides ◽

Rebaudioside A ◽

Carotenoid Concentration

In plants, phosphorus (P) uptake occurs via arbuscular mycorrhizal (AM) symbiosis and through plant roots. The phosphate concentration is known to affect colonization by AM fungi, and the effect depends on the plant species. Stevia rebaudiana plants are valuable sources of sweetener compounds called steviol glycosides (SGs), and the principal components of SGs are stevioside and rebaudioside A. However, a detailed analysis describing the effect of the phosphate concentration on the colonization of AM fungi in the roots and the relationship of these factors to the accumulation of SGs and photochemical performance has not been performed; such an analysis was the aim of this study. The results indicated that low phosphate concentrations (20 and 200 µM KH2PO4) induced a high percentage of colonization by Rhizophagus irregularis in the roots of S. rebaudiana, while high phosphate concentrations (500 and 1,000 µM KH2PO4) reduced colonization. The morphology of the colonization structure is a typical Arum-type mycorrhiza, and a mycorrhiza-specific phosphate transporter was identified. Colonization with low phosphate concentrations improved plant growth, chlorophyll and carotenoid concentration, and photochemical performance. The transcription of the genes that encode kaurene oxidase and glucosyltransferase (UGT74G1) was upregulated in colonized plants at 200 µM KH2PO4, which was consistent with the observed patterns of stevioside accumulation. In contrast, at 200 µM KH2PO4, the transcription of UGT76G1 and the accumulation of rebaudioside A were higher in noncolonized plants than in colonized plants. These results indicate that a low phosphate concentration improves mycorrhizal colonization and modulates the stevioside and rebaudioside A concentration by regulating the transcription of the genes that encode kaurene oxidase and glucosyltransferases, which are involved in stevioside and rebaudioside A synthesis in S. rebaudiana.

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Arbuscular Mycorrhizal Assessment of Ornamental Trees Grown in Tennessee Field Soils

HortScience ◽

10.21273/hortsci.37.5.778 ◽

2002 ◽

Vol 37 (5) ◽

pp. 778-782 ◽

Cited By ~ 2

Author(s):

W.E. Klingeman ◽

R.M. Augé ◽

P.C. Flanagan

Keyword(s):

Soil Ph ◽

Acer Rubrum ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Mycorrhizal Symbiosis ◽

Inoculum Potential ◽

Red Maple ◽

Trap Crop ◽

Tissue Samples ◽

Field Soils

Mycorrhizal symbiosis, a natural association between roots and certain soil fungi, can improve growth and increase stress resistance of many nursery crops. Field soils of four middle Tennessee and two eastern Tennessee nurseries were surveyed for their mycorrhizal inoculum potential (MIP), phosphorus (P) and potassium (K) concentrations, and soil pH. Arbuscular mycorrhizal (AM) fungi, which colonized seedlings of a Sorghum bicolor trap-crop, were recovered from all soils. Tissue samples were taken from young roots of three economically important tree species grown in nursery field soils: red maple (Acer rubrum L. `October Glory'), flowering dogwood (Cornus florida L. `Cherokee Princess'), and Kwanzan cherry (Prunus serrulata Lindl. `Kwanzan'). AM fungi, regardless of soil type, soil pH, or P or K concentration, had colonized young roots of all three species. Unless interested in establishing exotic mycorrhizae, ornamental nursery producers in Tennessee do not need to supplement field soils with these beneficial fungi.

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