scholarly journals Wheat Root and Rhizosphere Microbiome Structures and Functions Along Plant Growth

Author(s):  
Alla Usyskin-Tonne ◽  
Dror Minz ◽  
Yitzhak Hadar

Abstract Background Roots select their associated microbiome and affect its composition and activities through exudates that provide a nutrient-rich environment based on distance from the root. Root-exudation patterns depend on the plant's developmental stage. We followed field-grown wheat from emergence to spike maturation and compared the structure and functions of the microbiomes in two niches: adjacent, root-associated bacteria and the rhizosphere. The effects of growth stage on root-associated and rhizospheric communities structure and functions were investigated to enhance our understanding of plant–microbe interactions. Results A significant impact of wheat developmental stage during the transition from vegetative growth to spike formation was observed on structure and functions of both root-associated and rhizosphere microbiomes. On the root surface, abundance of the well-known wheat colonizers Proteobacteria and Actinobacteria decreased and increased, respectively, during spike formation, whereas abundance of Bacteroidetes was independent of spike formation. Three microbiome functional clusters were specifically associated with root proximity: (1) biofilm and sensorial movement; (2) antibiotic production and resistance; and (3) carbon biosynthesis, degradation and transporters, and amino acid biosynthesis and transporters. Interestingly, in the root-associated microbiome, genes related to all of these functions were influenced by spike formation. Abundance of genes related to nine other functions (lipopolysaccharide transporter and biosynthesis, beta-lactam resistance, metabolism of methane, alanine-aspartate-glutamate and arginine-proline, and biosynthesis of peptidoglycan, lysine and enediyne antibiotics) was significantly influenced by spike formation in both roots and rhizosphere. All of these genes were abundant in the rhizosphere, more so before spike formation when root exudation is high, supporting the notion that some of the root exudates are not fully utilized by the root-associated bacteria and subsequently diffuse into the surrounding soil, creating the rhizosphere. Conclusions We demonstrated functional division in the microbiome of the wheat root zone in both time and space: pre- and post-spike formation and root-associated vs. rhizospheric niches. The responses of the root microbiome were driven by both the plant and the microbial physiology and activities, both of which respond to environmental cues. These findings shed light on the dynamics of plant–microbe and microbe–microbe interactions in the root zone.

2021 ◽  
Vol 22 (21) ◽  
pp. 11948
Author(s):  
Alla Usyskin-Tonne ◽  
Yitzhak Hadar ◽  
Dror Minz

Root selection of their associated microbiome composition and activities is determined by the plant’s developmental stage and distance from the root. Total gene abundance, structure and functions of root-associated and rhizospheric microbiomes were studied throughout wheat growth season under field conditions. On the root surface, abundance of the well-known wheat colonizers Proteobacteria and Actinobacteria decreased and increased, respectively, during spike formation, whereas abundance of Bacteroidetes was independent of spike formation. Metagenomic analysis combined with functional co-occurrence networks revealed a significant impact of plant developmental stage on its microbiome during the transition from vegetative growth to spike formation. For example, gene functions related to biofilm and sensorial movement, antibiotic production and resistance and carbons and amino acids and their transporters. Genes associated with these functions were also in higher abundance in root vs. the rhizosphere microbiome. We propose that abundance of transporter-encoding genes related to carbon and amino acid, may mirror the availability and utilization of root exudates. Genes related to antibiotic resistance mechanisms were abundant during vegetative growth, while after spike formation, genes related to the biosynthesis of various antibiotics were enriched. This observation suggests that during root colonization and biofilm formation, bacteria cope with competitor’s antibiotics, whereas in the mature biofilm stage, they invest in inhibiting new colonizers. Additionally, there is higher abundance of genes related to denitrification in rhizosphere compared to root-associated microbiome during wheat growth, possibly due to competition with the plant over nitrogen in the root vicinity. We demonstrated functional and phylogenetic division in wheat root zone microbiome in both time and space: pre- and post-spike formation, and root-associated vs. rhizospheric niches. These findings shed light on the dynamics of plant–microbe and microbe–microbe interactions in the developing root zone.


2014 ◽  
Vol 1 (3) ◽  
pp. 57-61
Author(s):  
E. Kopylov

Aim. To study the specifi cities of complex inoculation of spring wheat roots with the bacteria of Azospirillum genus and Chaetomium cochliodes Palliser 3250, and the isolation of bacteria of Azospirillum genus, capable of fi xing atmospheric nitrogen, from the rhizospheric soil, washed-off roots and histoshere. Materials and meth- ods. The phenotypic features of the selected bacteria were identifi ed according to Bergi key. The molecular the polymerase chain reaction and genetic analysis was used for the identifi cation the bacteria. Results. It has been demonstrated that during the introduction into the root system of spring wheat the strain of A. brasilensе 102 actively colonizes rhizospheric soil, root surface and is capable of penetrating into the inner plant tissues. Conclusions. The soil ascomucete of C. cochliodes 3250 promotes better settling down of Azospirillum cells in spring wheat root zone, especially in plant histosphere which induces the increase in the content of chlorophyll a and b in the leaves and yield of the crop.


2020 ◽  
Author(s):  
Alla Usyskin-Tonne ◽  
Yitzhak Hadar ◽  
Uri Yermiyahu ◽  
Dror Minz

AbstractElevated CO2 stimulates plant growth and affects quantity and composition of root exudates, followed by response of its microbiome. Three scenarios representing nitrate fertilization regimes: limited (30 ppm), moderate (70 ppm) and excess nitrate (100 ppm) were compared under ambient and elevated CO2 (eCO2, 850 ppm) to elucidate their combined effects on root-surface-associated bacterial community abundance, structure and function. Wheat root-surface-associated microbiome structure and function, as well as soil and plant properties, were highly influenced by interactions between CO2 and nitrate levels. Relative abundance of total bacteria per plant increased at eCO2 under excess nitrate. Elevated CO2 significantly influenced the abundance of genes encoding enzymes, transporters and secretion systems. Proteobacteria, the largest taxonomic group in wheat roots (~ 75%), is the most influenced group by eCO2 under all nitrate levels. Rhizobiales, Burkholderiales and Pseudomonadales are responsible for most of these functional changes. A correlation was observed among the five gene-groups whose abundance was significantly changed (secretion systems, particularly type VI secretion system, biofilm formation, pyruvate, fructose and mannose metabolism). These changes in bacterial abundance and gene functions may be the result of alteration in root exudation at eCO2, leading to changes in bacteria colonization patterns and influencing their fitness and proliferation.


Author(s):  
Junnosuke Otaka ◽  
Guntur Venkata Subbarao ◽  
Hiroshi Ono ◽  
Tadashi Yoshihashi

AbstractTo control agronomic N losses and reduce environmental pollution, biological nitrification inhibition (BNI) is a promising strategy. BNI is an ecological phenomenon by which certain plants release bioactive compounds that can suppress nitrifying soil microbes. Herein, we report on two hydrophobic BNI compounds released from maize root exudation (1 and 2), together with two BNI compounds inside maize roots (3 and 4). On the basis of a bioassay-guided fractionation method using a recombinant nitrifying bacterium Nitrosomonas europaea, 2,7-dimethoxy-1,4-naphthoquinone (1, ED50 = 2 μM) was identified for the first time from dichloromethane (DCM) wash concentrate of maize root surface and named “zeanone.” The benzoxazinoid 2-hydroxy-4,7-dimethoxy-2H-1,4-benzoxazin-3(4H)-one (HDMBOA, 2, ED50 = 13 μM) was isolated from DCM extract of maize roots, and two analogs of compound 2, 2-hydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (HMBOA, 3, ED50 = 91 μM) and HDMBOA-β-glucoside (4, ED50 = 94 μM), were isolated from methanol extract of maize roots. Their chemical structures (1–4) were determined by extensive spectroscopic methods. The contributions of these four isolated BNI compounds (1–4) to the hydrophobic BNI activity in maize roots were 19%, 20%, 2%, and 4%, respectively. A possible biosynthetic pathway for zeanone (1) is proposed. These results provide insights into the strength of hydrophobic BNI activity released from maize root systems, the chemical identities of the isolated BNIs, and their relative contribution to the BNI activity from maize root systems.


2018 ◽  
Vol 56 (1) ◽  
pp. 361-380 ◽  
Author(s):  
Britt Koskella ◽  
Tiffany B. Taylor

Plant-associated bacteria face multiple selection pressures within their environments and have evolved countless adaptations that both depend on and shape bacterial phenotype and their interaction with plant hosts. Explaining bacterial adaptation and evolution therefore requires considering each of these forces independently as well as their interactions. In this review, we examine how bacteriophage viruses (phages) can alter the ecology and evolution of plant-associated bacterial populations and communities. This includes influencing a bacterial population's response to both abiotic and biotic selection pressures and altering ecological interactions within the microbiome and between the bacteria and host plant. We outline specific ways in which phages can alter bacterial phenotype and discuss when and how this might impact plant-microbe interactions, including for plant pathogens. Finally, we highlight key open questions in phage-bacteria-plant research and offer suggestions for future study.


2022 ◽  
Vol 12 ◽  
Author(s):  
Cécile Gruet ◽  
Daniel Muller ◽  
Yvan Moënne-Loccoz

Wheat, one of the major crops in the world, has had a complex history that includes genomic hybridizations between Triticum and Aegilops species and several domestication events, which resulted in various wild and domesticated species (especially Triticum aestivum and Triticum durum), many of them still existing today. The large body of information available on wheat-microbe interactions, however, was mostly obtained without considering the importance of wheat evolutionary history and its consequences for wheat microbial ecology. This review addresses our current understanding of the microbiome of wheat root and rhizosphere in light of the information available on pre- and post-domestication wheat history, including differences between wild and domesticated wheats, ancient and modern types of cultivars as well as individual cultivars within a given wheat species. This analysis highlighted two major trends. First, most data deal with the taxonomic diversity rather than the microbial functioning of root-associated wheat microbiota, with so far a bias toward bacteria and mycorrhizal fungi that will progressively attenuate thanks to the inclusion of markers encompassing other micro-eukaryotes and archaea. Second, the comparison of wheat genotypes has mostly focused on the comparison of T. aestivum cultivars, sometimes with little consideration for their particular genetic and physiological traits. It is expected that the development of current sequencing technologies will enable to revisit the diversity of the wheat microbiome. This will provide a renewed opportunity to better understand the significance of wheat evolutionary history, and also to obtain the baseline information needed to develop microbiome-based breeding strategies for sustainable wheat farming.


2002 ◽  
Vol 29 (5) ◽  
pp. 595 ◽  
Author(s):  
Sergey Shabala ◽  
Andrew Knowles

Oscillatory patterns in H+, K+, Ca2+ and Cl- uptake were observed at different regions of the root surface, including root hairs, using a non-invasive ion flux measuring technique (the MIFE™ technique). To our knowledge, this is the first report of ultradian oscillations in nutrient acquisition in the mature root zone. Oscillations of the largest magnitude were usually measured in the elongation region, 2–4 mm from the root apex. There were usually at least two oscillatory components present for each ion measured: fast, with periods of several minutes; and slow, with periods of 50–80 min. Even within the same functional zone, the periods of ion flux oscillations were significantly different, suggesting that they are driven by some internal mechanisms located in each cell rather than originating from one ‘central clock pacemaker’. There were also significant changes in the oscillatory characteristics (both periods and amplitudes) of fluxes from a single small cluster of cells over time. Analysis of phase shifts between oscillations in different ions suggested that rhythmic activity of a plasma membrane H+-pump may be central to observed rhythmic nutrient acquisition by plant roots. We discuss the possible adaptive significance of such an oscillatory strategy for root nutrient acquisition.


mSphere ◽  
2020 ◽  
Vol 5 (3) ◽  
Author(s):  
Ryan S. Nett ◽  
Huy Nguyen ◽  
Raimund Nagel ◽  
Ariana Marcassa ◽  
Trevor C. Charles ◽  
...  

ABSTRACT Gibberellin (GA) phytohormones are ubiquitous regulators of growth and developmental processes in vascular plants. The convergent evolution of GA production by plant-associated bacteria, including both symbiotic nitrogen-fixing rhizobia and phytopathogens, suggests that manipulation of GA signaling is a powerful mechanism for microbes to gain an advantage in these interactions. Although orthologous operons encode GA biosynthetic enzymes in both rhizobia and phytopathogens, notable genetic heterogeneity and scattered operon distribution in these lineages, including loss of the gene for the final biosynthetic step in most rhizobia, suggest varied functions for GA in these distinct plant-microbe interactions. Therefore, deciphering GA operon evolutionary history should provide crucial evidence toward understanding the distinct biological roles for bacterial GA production. To further establish the genetic composition of the GA operon, two operon-associated genes that exhibit limited distribution among rhizobia were biochemically characterized, verifying their roles in GA biosynthesis. This enabled employment of a maximum parsimony ancestral gene block reconstruction algorithm to characterize loss, gain, and horizontal gene transfer (HGT) of GA operon genes within alphaproteobacterial rhizobia, which exhibit the most heterogeneity among the bacteria containing this biosynthetic gene cluster. Collectively, this evolutionary analysis reveals a complex history for HGT of the entire GA operon, as well as the individual genes therein, and ultimately provides a basis for linking genetic content to bacterial GA functions in diverse plant-microbe interactions, including insight into the subtleties of the coevolving molecular interactions between rhizobia and their leguminous host plants. IMPORTANCE While production of phytohormones by plant-associated microbes has long been appreciated, identification of the gibberellin (GA) biosynthetic operon in plant-associated bacteria has revealed surprising genetic heterogeneity. Notably, this heterogeneity seems to be associated with the lifestyle of the microbe; while the GA operon in phytopathogenic bacteria does not seem to vary to any significant degree, thus enabling production of bioactive GA, symbiotic rhizobia exhibit a number of GA operon gene loss and gain events. This suggests that a unique set of selective pressures are exerted on this biosynthetic gene cluster in rhizobia. Through analysis of the evolutionary history of the GA operon in alphaproteobacterial rhizobia, which display substantial diversity in their GA operon structure and gene content, we provide insight into the effect of lifestyle and host interactions on the production of this phytohormone by plant-associated bacteria.


1965 ◽  
Vol 11 (3) ◽  
pp. 483-489 ◽  
Author(s):  
E. A. Peterson ◽  
J. W. Rouatt ◽  
H. Katznelson

The influence of soil moisture on the microbial population of rhizosphere soil and of the root surface (rhizoplane) of wheat was studied under controlled conditions. Fertile soil adjusted to 30%, 60%, and 90% of its moisture-holding capacity was used. Bacterial counts and numbers of specific "physiological groups" of bacteria all increased in the rhizosphere and the rhizoplane as soil moisture decreased. Taxonomic studies of the bacteria isolated from the rhizoplane showed a marked preponderance of species of Pseudomonas under conditions of low and intermediate soil moisture content. On the other hand species of Arthrobacter, Bacillus, and Cytophaga dominated the population at high soil moisture. Although the distribution of fungi on the roots was very similar for the low and intermediate moisture levels, there was some restriction of colonization at the high level. Species of Mortierella, Rhizopus, Chaetomium, Curvularia, and Helminthosporium were not represented among isolates from roots at high soil moisture and the relative incidence of species of Fusarium and Phoma decreased. However, high soil moisture favored root colonization by species of Rhizoctonia and sterile dark fungi.


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