Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere

The rhizosphere is strongly influenced by plant-derived phytochemicals exuded by roots and plant species exert a major selective force for bacteria colonizing the root-soil interface. We have previously shown that rhizobacterial recruitment is tightly regulated by plant genetics, by showing that natural variants of Arabidopsis thaliana support genotype-specific rhizobacterial communities while also releasing a unique blend of exudates at six weeks post-germination. To further understand how exudate release is controlled by plants, changes in rhizobacterial assemblages of two Arabidopsis accessions, Cvi and Ler where monitored throughout the plants'' life cycle. Denaturing gradient gel electrophoresis (DGGE) fingerprints revealed that bacterial communities respond to plant derived factors immediately upon germination in an accession-specific manner. Rhizobacterial succession progresses differently in the two accessions in a reproducible manner. However, as plants age, rhizobacterial and control bulk soil communities converge, indicative of an attenuated rhizosphere effect, which coincides with the expected slow down in the active release of root exudates as plants reach the end of their life cycle. These data strongly suggest that exudation changes during plant development are highly genotype-specific, possibly reflecting the unique, local co-evolutionary communication processes that developed between Arabidopsis accessions and their indigenous microbiota.Key words: rhizobacterial succession, rhizobacterial communities, natural variation, root exudates, Arabidopsis accessions     

Life cycle stage and water depth affect flooding-induced adventitious root formation in the terrestrial species Solanum dulcamara

Background and Aims Flooding can occur at any stage of the life cycle of a plant, but often adaptive responses of plants are only studied at a single developmental stage. It may be anticipated that juvenile plants may respond differently from mature plants, as the amount of stored resources may differ and morphological changes can be constrained. Moreover, different water depths may require different strategies to cope with the flooding stress, the expression of which may also depend on developmental stage. This study investigated whether flooding-induced adventitious root formation and plant growth were affected by flooding depth in Solanum dulcamara plants at different developmental stages.Methods Juvenile plants without pre-formed adventitious root primordia and mature plants with primordia were subjected to shallow flooding or deep flooding for 5 weeks. Plant growth and the timing of adventitious root formation were monitored during the flooding treatments.Key Results Adventitious root formation in response to shallow flooding was significantly constrained in juvenile S. dulcamara plants compared with mature plants, and was delayed by deep flooding compared with shallow flooding. Complete submergence suppressed adventitious root formation until up to 2 weeks after shoots restored contact with the atmosphere. Independent of developmental stage, a strong positive correlation was found between adventitious root formation and total biomass accumulation during shallow flooding.Conclusions The potential to deploy an escape strategy (i.e. adventitious root formation) may change throughout a plant’s life cycle, and is largely dependent on flooding depth. Adaptive responses at a given stage of the life cycle thus do not necessarily predict how the plant responds to flooding in another growth stage. As variation in adventitious root formation also correlates with finally attained biomass, this variation may form the basis for variation in resistance to shallow flooding among plants.     

Iron sulfide formation on root surfaces controlled by the life cycle of wild rice (<Emphasis Type="Italic">Zizania palustris</Emphasis>)

Iron sulfide plaques have been observed on roots of wild rice (Zizania palustris) and other wetland plants grown in sulfur-impacted freshwater ecosystems, but the mechanism of their formation and ramifications for plants have not been investigated. We exposed a model annual wetland plant, Zizania palustris, to elevated sulfate concentrations (3.1 mM) and quantified the development of iron oxide and iron sulfide precipitates on root surfaces throughout the plant life cycle. During the onset of seed production, root surfaces amended with sulfate transitioned within 1 week from iron (hydr)oxide plaques to iron sulfide plaques. During the same week, Fe(III) decreased on roots of plants not amended with sulfate but FeS did not accumulate. Prior to FeS accumulation, sulfate-amended plants had taken up the same amount of N as unamended plants. After FeS accumulation, total plant nitrogen did not increase further on sulfate-amended plants, indicating a cessation in nitrogen uptake, whereas total plant N continued to increase in unamended plants. Sulfate-amended plants produced fewer and lighter seeds with less nitrogen than unamended plants. FeS precipitation on roots may be associated with elevated sulfide and inhibited nitrogen uptake before the end of the plant’s life cycle, thus affecting the populations of this annual aquatic plant. We propose a mechanism by which a physiologically-induced decline in radial oxygen loss near the end of a plant’s life cycle initiates a precipitous decline in redox potential at the root surface and in adjacent porewater, initiating accumulation of iron sulfide plaques. These plaques could be an important locus for iron sulfide accumulation in wetland sediments.     

Dynamic root growth and architecture responses to limiting nutrient availability: linking physiological models and experimentation

In recent years the study of root phenotypic plasticity in response to sub-optimal environmental factors and the genetic control of these responses have received renewed attention. As a path to increased productivity, in particular for low fertility soils, several applied research projects worldwide target the improvement of crop root traits both in plant breeding and biotechnology contexts. To assist these tasks and address the challenge of optimizing root growth and architecture for enhanced mineral resource use, the development of realistic simulation models is of great importance. We review this research field from a modeling perspective focusing particularly on nutrient acquisition strategies for crop production on low nitrogen and low phosphorous soils. Soil heterogeneity and the dynamics of nutrient availability in the soil pose a challenging environment in which plants have to forage efficiently for nutrients in order to maintain their internal nutrient homeostasis throughout their life cycle. Mathematical models assist in understanding plant growth strategies and associated root phenes that have potential to be tested and introduced in physiological breeding programs. At the same time, we stress that it is necessary to carefully consider model assumptions and development from a whole plant-resource allocation perspective and to introduce or refine modules simulating explicitly root growth and architecture dynamics through ontogeny with reference to key factors that constrain root growth. In this view it is important to understand negative feedbacks such as plant–plant competition. We conclude by briefly touching on available and developing technologies for quantitative root phenotyping from lab to field, from quantification of partial root profiles in the field to 3D reconstruction of whole root systems. Finally, we discuss how these approaches can and should be tightly linked to modeling to explore the root phenome.     

根际微生物促进水稻氮利用的机制

根际微生物影响植物的生长及环境适应性。不同种属、不同种群的植物影响其环境微生物群落;反之,根际微生物也影响宿主植物生长发育与生态适应性。植物与根际微生物的互作现象及其机制,是生命科学研究关注的热点,也是农业微生物利用的关键问题。近期,中国科学家在该领域取得了突破性进展。通过对不同籼稻(Oryza sativa subsp. indica)和粳稻(O. sativa subsp. japonica)品种的根际微生物组进行研究,发现籼稻根际比粳稻根际富集更多参与氮代谢的微生物群落,且该现象与硝酸盐转运蛋白基因NRT1.1B在籼粳之间的自然变异相关联。通过对籼稻接种籼稻根际特异富集的微生物群体可以提高前者对有机氮的利用,促进其生长。该研究揭示了籼稻和粳稻根际微生物分化的分子基础,展示了利用根际微生物提高水稻营养高效吸收的应用前景。     

根际微生物促进水稻氮利用的机制

根际微生物影响植物的生长及环境适应性。不同种属、不同种群的植物影响其环境微生物群落; 反之, 根际微生物也影响宿主植物生长发育与生态适应性。植物与根际微生物的互作现象及其机制, 是生命科学研究关注的热点, 也是农业微生物利用的关键问题。近期, 中国科学家在该领域取得了突破性进展。通过对不同籼稻(Oryza sativa subsp. indica)和粳稻(O. sativa subsp. japonica)品种的根际微生物组进行研究, 发现籼稻根际比粳稻根际富集更多参与氮代谢的微生物群落, 且该现象与硝酸盐转运蛋白基因NRT1.1B在籼粳之间的自然变异相关联。通过对籼稻接种籼稻根际特异富集的微生物群体可以提高前者对有机氮的利用, 促进其生长。该研究揭示了籼稻和粳稻根际微生物分化的分子基础, 展示了利用根际微生物提高水稻营养高效吸收的应用前景。     

Rhizobien in der Pflanzenmikrobiota

Rhizobia in the plant microbiota The plant microbiota is of critical importance for plant growth and survival in soil. To explore mechanisms underlying plant‐microbiota interactions, defined commensal communities can be composed from microbiota culture collections and co‐cultivated with germ‐free plants to determine their impact on plant growth and health. The order Rhizobiales belongs to the core microbiota and includes nitrogen‐fixing bacteria that are known to engage in symbiotic interactions with legumes. Compatible host‐symbiont pairs are needed for a functional symbiosis, which involves the activation of highly specialized and interdependent signaling pathways between the two partners. Comparative genome analysis of more than 1,300 legume symbionts and rhizobial root commensals from non‐leguminous plants revealed that the most recent common ancestor of rhizobia lacked the gene repertoire needed for symbiosis and was able to colonize roots of a wide variety of plants. During evolution, key symbiosis genes were acquired multiple independent times by commensals belonging to different families of the Rhizobiales order.     

Plant microbiota modified by plant domestication

Human life became largely dependent on agricultural products after distinct crop-domestication events occurred around 10,000 years ago in different geographical sites. Domestication selected suitable plants for human agricultural practices with unexpected consequences on plant microbiota, which has notable effects on plant growth and health. Among other traits, domestication has changed root architecture, exudation, or defense responses that could have modified plant microbiota. Here we present the comparison of reported data on the microbiota from widely consumed cereals and legumes and their ancestors showing that different bacteria were found in domesticated and wild plant microbiomes in some cases. Considering the large variability in plant microbiota, adequate sampling efforts and function-based approaches are needed to further support differences between the microbiota from wild and domesticated plants. The study of wild plant microbiomes could provide a valuable resource of unexploited beneficial bacteria for crops.     

Root cooling strongly affects diel leaf growth dynamics,water and carbohydrate relations in Ricinus communis

In laboratory and greenhouse experiments with potted plants, shoots and roots are exposed to temperature regimes throughout a 24 h (diel) cycle that can differ strongly from the regime under which these plants have evolved. In the field, roots are often exposed to lower temperatures than shoots. When the root‐zone temperature in Ricinus communis was decreased below a threshold value, leaf growth occurred preferentially at night and was strongly inhibited during the day. Overall, leaf expansion, shoot biomass growth, root elongation and ramification decreased rapidly, carbon fluxes from shoot to root were diminished and carbohydrate contents of both root and shoot increased. Further, transpiration rate was not affected, yet hydrostatic tensions in shoot xylem increased. When root temperature was increased again, xylem tension reduced, leaf growth recovered rapidly, carbon fluxes from shoot to root increased, and carbohydrate pools were depleted. We hypothesize that the decreased uptake of water in cool roots diminishes the growth potential of the entire plant – especially diurnally, when the growing leaf loses water via transpiration. As a consequence, leaf growth and metabolite concentrations can vary enormously, depending on root‐zone temperature and its heterogeneity inside pots.     

Interaction of Combined Nitrogen with the Expression of Root-Associated Nitrogenase Activity in Grasses and with the Development of N(2) Fixation in Soybean (Glycine max L. Merr.)

Soluble root N concentrations of corn, sorghum, pearl millet, rice, wild rice, and soybeans were determined and related to measurements of nitrogenase activity and changes in availability of combined N to plants. In corn, sorghum, and pearl millet, applications of fertilizer N increased soluble root N concentrations, but root-associated nitrogenase activity was negligible in control and treated plants. Applications of NH₄NO₃ to rice increased the water soluble root N concentrations and inhibited root-associated nitrogenase activity. In wild rice, root-associated nitrogenase activity was absent during vegetative growth and developed at the reproductive growth stage. The soluble root N concentration decreased progressively as wild rice grew indicating that the availability of combined N in the root environment declined. Therefore, development of nitrogenase activity in wild rice is associated with the change in availability of combined N in the root environment. The development of nitrogenase activity in wild rice was probably not due to colonization of roots by N₂-fixing bacteria because most probable numbers of recovery did not significantly vary throughout the plants' growth cycle. In field-grown soybeans with or without fertilizer N application, we also observed a relationship between a decrease in soluble root N concentration and the development of nitrogenase activity.     

Effect of long-term organic and mineral fertilization strategies on rhizosphere microbiota assemblage and performance of lettuce

Long-term agricultural fertilization strategies gradually change soil properties including the associated microbial communities. Cultivated crops recruit beneficial microbes from the surrounding soil environment via root exudates. In this study, we aimed to investigate the effects of long-term fertilization strategies across field sites on the rhizosphere prokaryotic (Bacteria and Archaea) community composition and plant performance. We conducted growth chamber experiments with lettuce (Lactuca sativa L.) cultivated in soils from two long-term field experiments, each of which compared organic versus mineral fertilization strategies. 16S rRNA gene amplicon sequencing revealed the assemblage of a rhizosphere core microbiota shared in all lettuce plants across soils, going beyond differences in community composition depending on field site and fertilization strategies. The enhanced expression of several plant genes with roles in oxidative and biotic stress signalling pathways in lettuce grown in soils with organic indicates an induced physiological status in plants. Lettuce plants grown in soils with different fertilization histories were visibly free of stress symptoms and achieved comparable biomass. This suggests a positive aboveground plant response to belowground plant–microbe interactions in the rhizosphere. Besides effects of fertilization strategy and field site, our results demonstrate the crucial role of the plant in driving rhizosphere microbiota assemblage.     

Recently duplicated sesterterpene (C25) gene clusters in Arabidopsis thaliana modulate root microbiota

Land plants co-speciate with a diversity of continually expanding plant specialized metabolites(PSMs) and root microbial communities(microbiota). Homeostatic interactions between plants and root microbiota are essential for plant survival in natural environments. A growing appreciation of microbiota for plant health is fuelling rapid advances in genetic mechanisms of controlling microbiota by host plants. PSMs have long been proposed to mediate plant and single microbe interactions. However,the effects of PSMs, especially those evolutionarily new PSMs, on root microbiota at community level remain to be elucidated.Here, we discovered sesterterpenes in Arabidopsis thaliana, produced by recently duplicated prenyltransferase-terpene synthase(PT-TPS) gene clusters, with neo-functionalization. A single-residue substitution played a critical role in the acquisition of sesterterpene synthase(sesterTPS) activity in Brassicaceae plants. Moreover, we found that the absence of two root-specific sesterterpenoids, with similar chemical structure, significantly affected root microbiota assembly in similar patterns. Our results not only demonstrate the sensitivity of plant microbiota to PSMs but also establish a complete framework of host plants to control root microbiota composition through evolutionarily dynamic PSMs.     

The root microbiota—a fingerprint in the soil?

Background

The root system of a plant is known to host a wide diversity of microbes that can be essential or detrimental to the plant. Microbial ecologists have long struggled to understand what factors structure the composition of these communities. An overlooked part of the microbial community succession in root systems has been the potential for individual variation among plants shaped by early colonisation events such as microbial exposure of the seed inside the parent plant and during dispersal.

Scope

In this review we outline life events of the plant that can affect the composition of its root microbiota and relate ecological theory of community assembly to the formation of the root microbiota.

Conclusion

All plants are exposed to environmental conditions and events throughout their lifetime that shape their phenotype. The microbial community associated with the plant is ultimately an extension of this phenotype. Therefore, only by following a plant from its origin inside the flower to senescence, can we fully understand how the associated microbial community was assembled and what determined its composition.     

The decline in N2 fixation rate in common bean with the onset of pod-filling: Fact or artifact

It is not clear to what extent genetic, environmental and measurement factors are responsible for the commonly reported decline in nitrogenase activity with the onset of pod-filling in grain legumes. We address this question by observing nitrogenase activity and assimilate partitioning throughout the life span of an indeterminate variety of common bean (GN 1140) under controlled-environment and field conditions. Nitrogenase activity per plant was maintained well into pod-filling in GN 1140 under high-light conditions in growth cabinets. In contrast, plants exposed to a gradual reduction in light intensity during early reproductive growth had a decline in nitrogenase activity on a whole plant basis with the onset of pod-filling. However, the decline was due to an inability to maintain nodule growth, rather than a decrease in specific nitrogenase activity. Under field conditions, acetylene reduction assay of root crowns appeared to indicate a rapid decline in nitrogenase activity with the onset of pod-filling in GN 1140. This decline was not correlated with the water status of the soil or the plant. In contrast, acetylene reduction activity of root cores taken from outside the root crown region (non-crown) and N accumulation by above-ground biomass during pod-filling suggested that whole plant nitrogenase activity was maintained longer than that indicated by root crown assays. We conclude that although the occurrence of a decline in nitrogenase activity with the onset of pod-filling in grain legumes can be genetically determined, in many cases the decline can be the result of growing conditions and improper measurement techniques.     

The rice histone methylation regulates hub species of the root microbiota

Plants have a close relationship with their root microbiota, which comprises a complex microbial network. Histone methylation is an important epigenetic modification influencing multiple plant traits; however, little is known about the role of plant histone methylation in the assembly and network structure of the root microbiota. In this study, we established that the rice (Oryza sativa) histone methylation regulates the structure and composition of the root microbiota, especially the hub species in the microbial network. DJ-jmj703 (defective in histone H3K4 demethylation) and ZH11-sdg714 (defective in H3K9 methylation) showed significant different root microbiota compared with the corresponding wild types at the phylum and family levels, with a consistent increase in the abundance of Betaproteobacteria and a decrease in the Firmicutes. In the root microbial network, 35 of 44 hub species in the top 10 modules in the tested field were regulated by at least one histone methylation-related gene. These observations establish that the rice histone methylation plays a pivotal role in regulating the assembly of the root microbiota, providing insights into the links between plant epigenetic regulation and root microbiota.     

NtGNL1 is involved in embryonic cell division patterning, root elongation, and pollen tube growth in tobacco

The function of the ARF-GEF family has drawn great attention recently, especially GNOM and GNL1, owing to their important role in plant development. A homolog of GBF was identified in Nicotiana tabacum, named NtGNL1, which is ubiquitously expressed throughout the tobacco life cycle. In NtGNL1 RNAi plants, irregular orientation of cell division and asynchronous cell development during early embryogenesis disrupted the symmetry of the developing embryo. In addition, root growth in transgenic lines was significantly slower than that in wild-type plants, although the structure of the root tip was largely intact. Pollen germination and pollen tube growth were also inhibited in the transgenic lines, and the tip of the pollen tube presented various aberrant morphologies in one of the transgenic lines. The phenotypes of different NtGNL1 RNAi transgenic lines suggest that the NtGNL1 is likely to be involved not only in embryogenesis and postembryonic development, but also in sexual reproduction; thus, NtGNL1 may play multiple and critical roles in plant development.     

Long-term responses of Melilotus segetalis to salinity. I. Growth and partitioning

Annual sweetclover plants [Melilotus segetalis (Brot) Ser.] were grown for a complete life cycle with and without saline (NaCl treatment of CE=15 dS m⁻¹). Growth and partitioning analyses were performed. Sequential harvests (every 15 d) during the life cycle, and separation of plant material into roots, stems, petioles, leaves and reproductive structures were carried out Salt treatment reduced growth during the early and middle stages of the life of the plant, but did not significantly affect RGR in the reproductive phase. The root–shoot allometric coefficient of salinized plants in the generative phase decreased more than in control plants. We suggest that salinity-induced growth reduction in M. segetalis was primarily a result of a lower unit leaf rate (ULR) despite an increased leaf area ratio (LAR). Earlier flowering, higher biomass allocation to shoot and greater reproductive investment, but similar relative growth rate (RGR), were some of the main characteristics of salt-stressed plants compared to controls during the reproductive phase, these apparently being associated with increased sink strength caused by developing flowers and fruits.