Plant hormones as signals in arbuscular mycorrhizal symbiosis

Abstract

Arbuscular mycorrhizal (AM) fungi are non-specific symbionts developing mutual and beneficial symbiosis with most terrestrial plants. Because of the obligatory nature of the symbiosis, the presence of the host plant during the onset and proceeding of symbiosis is necessary. However, AM fungal spores are able to germinate in the absence of the host plant. The fungi detect the presence of the host plant through some signal communications. Among the signal molecules, which can affect mycorrhizal symbiosis are plant hormones, which may positively or adversely affect the symbiosis. In this review article, some of the most recent findings regarding the signaling effects of plant hormones, on mycorrhizal fungal symbiosis are reviewed. This may be useful for the production of plants, which are more responsive to mycorrhizal symbiosis under stress.     

丛枝菌根真菌脂类代谢对共生信号调控的响应和反馈

丛枝菌根(AM)真菌是自然生态系统中分布最为广泛的真菌之一,在自然界物质循环和能量流动中发挥着重要作用。经过长期的协同进化,AM真菌和宿主植物之间形成了完美的互惠互利的共生关系,而真菌的脂类代谢可能是揭示共生秘密的关键所在。本文综述了AM真菌脂类代谢在共生关系建立和维持中关键作用的最新研究进展,重点探讨了AM真菌脂类代谢对共生信号调控的响应和反馈机制,主要包括:AM真菌脂类存储和释放对共生和非共生状态的响应,以及脂类代谢产物变化与共生营养传递之间的关系;脂类分解过程在共生建立初期对信号分子调控发生的响应,以及相应的物质转化和能量代谢;菌根共生互惠互利关系维持中,真菌脂类代谢与信号分子交流通道的相互渗透和影响。本文对于理解菌根共生机制,促进菌根在生产中的应用具有促进作用。     

Development of the arbuscular mycorrhizal symbiosis

The arbuscular mycorrhizal (AM) symbiosis formed between plant roots and fungi is one of the most widespread symbiotic associations found in plants, yet our understanding of events underlying its development are limited. The recent integration of biochemical, molecular and genetic approaches into analyses of the symbiosis is providing new insights into various aspects of its development. In the past year there have been advances in our understanding of the signals required for the formation of appressoria, the molecular changes in the root in response to colonisation, and components of the signal transduction pathways common to both the AM and Rhizobium symbioses.     

Functional complementarity in the arbuscular mycorrhizal symbiosis

The causes and consequences of biodiversity are central themes in ecology. Perhaps one reason for much of the current interest in biodiversity is the belief that the loss of species (by extinction) or their gain (by invasion) will significantly influence ecosystem function. Arbuscular mycorrhizal (AM) fungi are components of most terrestrial ecosystems and, while many research programs have shown that variability among species or isolates of AM fungi does occur (Giovannetti & Gianinazzi-Pearson, 1994), the basis for this variability and its consequences to the function of communities and ecosystems remains largely unexplored. Smith et al . (pp. 357–366 in this issue) now show clearly that ecologically significant functional diversity exists among AM fungal species in the regions of the soil from which they absorb phosphate, and their results suggest that such diversity may have significant ecological consequences.     

Molecular genetics of the arbuscular mycorrhizal symbiosis

During arbuscular mycorrhiza (AM) development, fungal hyphae grow throughout root epidermal, exodermal and cortical cell layers to reach the inner cortex where the symbiosis' functional units, the arbuscles, develop. Three essential components of a plant signalling network, a receptor-like kinase, a predicted ion-channel and a calmodulin-dependent protein kinase have been identified. A detailed morphological study of symbiotic plant mutants revealed that different subsets of plant genes support the progress of fungal infection in successive root cell layers. Moreover, evidence of a diffusible fungal signalling factor that triggers gene activation in the root has recently been obtained.     

丛枝菌根真菌-豆科植物-根瘤菌共生体系的研究进展

丛枝菌根真菌（Arbuscular Mycorrhizal Fungi,AMF）-豆科植物-根瘤菌（Rhizobia）三者形成的共生体。是植物与微生物共生中的一种特殊类型。本文对这种共生体中微生物与植物之间的营养关系;AMF和根瘤菌双接种豆科植物的效应以及影响双接种效应的因素;AMF和根瘤菌在与豆科植物形成共生过程中的分子互作机制等进行了综述。同时对这种共生体还需进一步研究的问题及其在基础研究和实践应用方面的前景进行了讨论。     

Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation

High concentrations of heavy metals (HM) in the soil have detrimental effects on ecosystems and are a risk to human health as they can enter the food chain via agricultural products or contaminated drinking water. Phytoremediation, a sustainable and inexpensive technology based on the removal of pollutants from the environment by plants, is becoming an increasingly important objective in plant research. However, as phytoremediation is a slow process, improvement of efficiency and thus increased stabilization or removal of HMs from soils is an important goal. Arbuscular mycorrhizal (AM) fungi provide an attractive system to advance plant-based environmental clean-up. During symbiotic interaction the hyphal network functionally extends the root system of their hosts. Thus, plants in symbiosis with AM fungi have the potential to take up HM from an enlarged soil volume. In this review, we summarize current knowledge about the contribution of the AM symbiosis to phytoremediation of heavy metals.     

Seasonal dynamics of arbuscular mycorrhizal fungal communities in roots in a seminatural grassland

Symbiotic arbuscular mycorrhizal fungi (AMF) have been shown to influence both the diversity and productivity of grassland plant communities. These effects have been postulated to depend on the differential effects of individual mycorrhizal taxa on different plant species; however, so far there are few detailed studies of the dynamics of AMF colonization of different plant species. In this study, we characterized the communities of AMF colonizing the roots of two plant species, Prunella vulgaris and Antennaria dioica, in a Swedish seminatural grassland at different times of the year. The AMF small subunit rRNA genes were subjected to PCR, cloning, sequencing, and phylogenetic analysis. Nineteen discrete sequence types belonging to Glomus groups A and B and to the genus Acaulospora were distinguished. No significant seasonal changes in the species compositions of the AMF communities as a whole were observed. However, the two plant species hosted significantly different AMF communities. P. vulgaris hosted a rich AMF community throughout the entire growing season. The presence of AMF in A. dioica decreased dramatically in autumn, while an increased presence of Ascomycetes species was detected.     

Programming good relations--development of the arbuscular mycorrhizal symbiosis

The majority of plants live in symbiotic associations with fungi or bacteria that improve their nutrition. Critical steps in a symbiosis are mutual recognition and subsequently the establishment of an intimate association, which involves the penetration of plant tissues and, in many cases, the invasion of individual host cells by the microbial symbiont. Recent advances revealed that in the arbuscular mycorrhizal symbiosis with soil fungi of the order Glomeromycota, plant-derived signals attract fungal hyphae and stimulate their growth. Upon physical attachment of the fungal symbiont to the root surface, an active plant developmental program prepares the epidermal cells for penetration by the fungus. Thus, plants actively help symbiotic fungi to colonize their roots rather than just tolerating them.     

Inner Mongolian steppe arbuscular mycorrhizal fungal communities respond more strongly to water availability than to nitrogen fertilization

Plant community productivity and species composition are primarily constrained by water followed by nitrogen (N) availability in the degraded semi‐arid grasslands of Inner Mongolia. However, there is a lack of knowledge on how long‐term N addition and water availability interact to influence the community structure of arbuscular mycorrhizal (AM) fungi, and whether AM fungi contribute to the recovery of degraded grasslands. Soils and roots of the dominant plant species Stipa grandis and Agropyron cristatum were sampled under two water levels and N) rates after 8 years. The abundance and diversity of AM fungi remained relatively resilient after the long‐term addition of water and N. Variation in the AM fungal communities in soils and roots were affected primarily by watering. AM fungal abundance and operational taxonomic unit (OTU) richness were significantly correlated with average aboveground net primary productivity and biomass of plant functional groups. Hyphal length density was significantly correlated with plant richness, the average biomass of S. grandis and perennial forbs. Both water and plant biomass had a considerable influence on the AM fungal assemblages. The tight linkages between AM fungi with aboveground plant productivity highlight the importance of plant–microbe interactions in the productivity and sustainability of these semi‐arid grassland ecosystems.     

Seasonality of arbuscular mycorrhizal symbiosis and dark septate endophytes in a grassland site in southwest China

Arbuscular mycorrhizal and dark septate endophytic fungal colonization in a grassland in Kunming, southwest China, was investigated monthly over one year. All plant roots surveyed were co-colonized by arbuscular mycorrhizal and dark septate endophytic fungi in this grassland. Both arbuscular mycorrhizal and dark septate endophytic fungal colonization fluctuated significantly throughout the year, and their seasonal patterns were different in each plant species. The relationships between environmental (climatic and edaphic) factors and fungal colonization were also studied. Correlation analysis demonstrated that arbuscular mycorrhizal colonization was significantly correlative with environmental factors (rainfall, sunlight hours, soil P, etc.), but dark septate endophytic fungal colonization was only correlative with relative humidity and sunlight hours.     

Autofluorescence detection of arbuscular mycorrhizal fungal structures in palm roots: an underestimated experimental method

The aim of this study was to reassess the use of autofluorescence for evaluating AM colonization in mycorrhizal roots in the light of criticisms of this method that affirmed that only metabolically inactive arbuscules autofluoresce. It was also investigated whether other mycorrhizal structures, such as hyphae, vesicles and spores, could be detected by autofluorescence, and whether the autofluorescence pattern of AM fungal structures could be exploited methodologically, for example, in the detection and sorting of spores by flow cytometry. Mycorrhizal roots of the palm species Brahea armata, Chamaerops humilis, Phoenix canariensis and Phoenix dactylifera were sectioned and observed by means of fluorescence microscopy. In addition, fungal structures isolated from mycorrhizal roots of P. dactylifera were examined. The same root sections and isolated fungal structures were subjected to vital staining with nitro blue tetrazolium to determine their metabolic state (active or inactive). Moreover, spores of Glomus intraradices, and Glomus clarum were studied by epifluorescence and flow cytometry. Mycorrhizal whole roots of Medicago sativa were also assessed by autofluorescence detection. In contrast to previous reports, the results presented in this paper clearly demonstrate that all fungal structures, both intra- and extraradical, autofluoresced under blue light excitation, regardless of their state (dead or alive). Some arbuscules isolated from roots and mature spores showed further autofluorescence under green light excitation. The source of the autofluorescence was localized in the fungal cell wall. It was shown that AM spores can be detected by flow cytometry. The results support the use of autofluorescence for the evaluation of AM colonization, at least in palm species, and refute previous criticisms of the method.     

The arbuscular mycorrhizal symbiosis links N mineralization to plant demand

Arbuscular mycorrhizal (AM) fungi facilitate inorganic N (NH₄ ⁺ or NO₃ ⁻) uptake by plants, but their role in N mobilization from organic sources is unclear. We hypothesized that arbuscular mycorrhizae enhance the ability of a plant to use organic residues (ORs) as a source of N. This was tested under controlled glasshouse conditions by burying a patch of OR in soil separated by 20-μm nylon mesh so that only fungal hyphae can pass through it. The fate of the N contained in the OR patch, as influenced by Glomus claroideum, Glomus clarum, or Glomus intraradices over 24 weeks, was determined using ¹⁵N as a tracer. AM fungal species enhanced N mineralization from OR to different levels. N recovery and translocation to Russian wild rye by hyphae reached 25% of mineralized N in G. clarum, which was most effective despite its smaller extraradical development in soil. Mobilization of N by G. clarum relieved plant N deficiency and enhanced plant growth. We show that AM hyphae modify soil functioning by linking plant growth to N mineralization from OR. AM species enhance N mineralization differentially leading to species-specific changes in the quality of the soil environment (soil C-to-N ratio) and structure of the soil microbial community.     

Preference,specificity and cheating in the arbuscular mycorrhizal symbiosis

Arbuscular mycorrhizal symbioses are mutualistic interactions between fungi and most plants. There is considerable interest in this symbiosis because of the strong nutritional benefits conferred to plants and its influence on plant diversity. Until recently, the symbiosis was assumed to be unspecific. However, two studies have now revealed that although it can be largely unspecific with the fungal community composition changing seasonally, in certain ecosystems it can also be highly specific and might potentially allow plants to cheat the arbuscular mycorrhizal network that connects plants below ground.