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 ◽  
...  

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.

2021 ◽  
Author(s):  
Peng Wang ◽  
Roxane Snijders ◽  
Wouter Kohlen ◽  
Jieyu Liu ◽  
Ton Bisseling ◽  
...  

AbstractTo acquire sufficient mineral nutrients such as phosphate (Pi) from the soil, most plants engage in a symbiosis with arbuscular mycorrhizal (AM) fungi. Attracted by plant-secreted strigolactones, the fungi colonize the roots and form highly-branched hyphal structures called arbuscules inside inner cortex cells. It is essential that the host plant controls 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 lifetime is far from understood. Here, we show that Medicago truncatula SPX-domain containing proteins SPX1 and SPX3 regulate root phosphate starvation responses as well as fungal colonization and arbuscule degradation. SPX1 and SPX3 are induced upon phosphate starvation but become restricted to arbuscule-containing cells upon establishment of the symbiosis. Under Pi-limiting conditions they facilitate the expression of the strigolactone biosynthesis gene DWARF27, which correlates with increased fungal branching by root exudates and increased root colonization. Later, in the arbuscule-containing cells SPX1 and SPX3 redundantly control the timely degradation of arbuscules. This regulation does not seem to involve direct interactions with known transcriptional regulators of arbuscule degradation. We propose a model where SPX1 and SPX3 control arbuscule degeneration in a Pi-dependent manner via a yet-to-identify negative regulator.


2010 ◽  
Vol 23 (7) ◽  
pp. 915-926 ◽  
Author(s):  
Anja Branscheid ◽  
Daniela Sieh ◽  
Bikram Datt Pant ◽  
Patrick May ◽  
Emanuel A. Devers ◽  
...  

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.


Author(s):  
Javier Puy ◽  
Carlos Perez Carmona ◽  
Inga Hiiesalu ◽  
Maarja Opik ◽  
Mari Moora ◽  
...  

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.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Manoj-Kumar Arthikala ◽  
Kalpana Nanjareddy ◽  
Lourdes Blanco ◽  
Xóchitl Alvarado-Affantranger ◽  
Miguel Lara

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.


Botany ◽  
2014 ◽  
Vol 92 (4) ◽  
pp. 241-251 ◽  
Author(s):  
Ylva Lekberg ◽  
Roger T. Koide

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.


2021 ◽  
Vol 7 (8) ◽  
pp. 671
Author(s):  
Xiao Lou ◽  
Xiangyu Zhang ◽  
Yu Zhang ◽  
Ming Tang

The simultaneous effects of arbuscular mycorrhizal (AM) fungi and abscisic acid (ABA) on the tolerance of plants to heavy metal (HM) remain unclear. A pot experiment was carried out to clarify the effects of simultaneous applications of AM fungi and ABA on plant growth, Zn accumulation, endogenous ABA contents, proline metabolism, and the oxidative injury of black locust (Robinia pseudoacacia L.) exposed to excess Zn stress. The results suggested that exogenously applied ABA positively enhanced AM colonization, and that the growth of plants only with AM fungi was improved by ABA application. Under Zn stress, AM inoculation and ABA application increased the ABA content in the root/leaf (increased by 48–172% and 92%, respectively) and Zn content in the root/shoot (increased by 63–152% and 61%, respectively) in AM plants, but no similar trends were observed in NM plants. Additionally, exogenous ABA addition increased the proline contents of NM roots concomitantly with the activities of the related synthases, whereas it reduced the proline contents and the activity of Δ1-pyrroline-5-carboxylate synthetase in AM roots. Under Zn stress, AM inoculation and ABA application decreased H2O2 contents and the production rate of O2, to varying degrees. Furthermore, in the roots exposed to Zn stress, AM inoculation augmented the activities of SOD, CAT, POD and APX, and exogenously applied ABA increased the activities of SOD and POD. Overall, AM inoculation combined with ABA application might be beneficial to the survival of black locust under Zn stress by improving AM symbiosis, inhibiting the transport of Zn from the roots to the shoots, increasing the distribution of ABA in roots, and stimulating antioxidant defense systems.


Cells ◽  
2019 ◽  
Vol 8 (5) ◽  
pp. 490 ◽  
Author(s):  
Yi Zhang ◽  
Lizong Hu ◽  
Deshui Yu ◽  
Kedong Xu ◽  
Ju Zhang ◽  
...  

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.


2022 ◽  
Vol 5 (1) ◽  
Author(s):  
Sachiko Tanaka ◽  
Kayo Hashimoto ◽  
Yuuki Kobayashi ◽  
Koji Yano ◽  
Taro Maeda ◽  
...  

AbstractArbuscular mycorrhizal (AM) symbiosis is a mutually beneficial interaction between fungi and land plants and promotes global phosphate cycling in terrestrial ecosystems. AM fungi are recognised as obligate symbionts that require root colonisation to complete a life cycle involving the production of propagules, asexual spores. Recently, it has been shown that Rhizophagus irregularis can produce infection-competent secondary spores asymbiotically by adding a fatty acid, palmitoleic acid. Furthermore, asymbiotic growth can be supported using myristate as a carbon and energy source for their asymbiotic growth to increase fungal biomass. However, the spore production and the ability of these spores to colonise host roots were still limited compared to the co-culture of the fungus with plant roots. Here we show that a combination of two plant hormones, strigolactone and jasmonate, induces the production of a large number of infection-competent spores in asymbiotic cultures of Rhizophagus clarus HR1 in the presence of myristate and organic nitrogen. Inoculation of asymbiotically-generated spores promoted the growth of host plants, as observed for spores produced by symbiotic culture system. Our findings provide a foundation for the elucidation of hormonal control of the fungal life cycle and the development of inoculum production schemes.


2020 ◽  
Author(s):  
Dayakar Govindu ◽  
Anusha Duvva ◽  
Srinivas Podeti

Arbuscular mycorrhizal (AM) association is the most common symbiotic association of plants with microbes. AM fungi occur in the majority of natural habitats and they provide a range of important biological services, in particular by improving plant nutrition, abiotic resistance, and soil structure and fertility. AM fungi also interact with most crop varieties and forest plants. The possible benefit of AM fungi in forestry can be achieved through a combination of inoculum methods. The mycorrhizal inoculum levels in the soil and their colonization in different forest plant roots which leads to reduce the fertilizers, pathogen effects and fungicides and to protect topsoil, soil erosion, and water-logging. Currently, several reports were suggested that AM symbiosis can improve the potential for different plant species. Two steps could be used to produce high yielding of different plant biomass that would be both mycorrhizal dependency and suitability for sowing into the field with high inoculum levels Therefore, the wide-scale inoculation of AM fungi on forest trees will become economically important. The successful research is required in the area of mass production of AM fungal inoculum and AM fungi associated with roots which will contribute to sustainable forestry.


2021 ◽  
Author(s):  
Kyoichi Kodama ◽  
Mélanie K. Rich ◽  
Akiyoshi Yoda ◽  
Shota Shimazaki ◽  
Xiaonan Xie ◽  
...  

AbstractIn flowering plants, carotenoid-derived strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), a previously unidentified SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating that it is ancestral in land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders M. paleacea cells BSB-responsive. These results suggest that BSB is not perceived by M. paleacea cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.


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