An official website of the United States government
Abstract Plants produce an astonishingly diverse array of specialized metabolites. A crucial step in understanding the origin of such chemodiversity is describing how chemodiversity manifests across the spatial and ontogenetic scales relevant to plant–biotic interactions.Focusing on 21 sympatric species ofPsychotriaandPalicourea sensu lato(Rubiaceae), we describe patterns of specialized metabolite diversity across spatial and ontogenetic scales using a combination of field collections, untargeted metabolomics, and ecoinformatics. We compare α, β, and γ diversity of specialized metabolites in expanding leaves, unripe pulp, immature seed, ripe pulp, mature seed, and fine roots.Within species, fruit tissues from across ontogenetic stages had ≥α diversity than leaves, and ≤β diversity than leaves. Pooled across species, fruit tissues and ontogenetic stages had the highest γ diversity of all organs, and fruit tissues and ontogenetic stages combined had a higher incidence of organ‐specific mass spectral features than leaves. Roots had ≤α diversity than leaves and the lowest β and γ diversity of all organs. Phylogenetic correlations of chemical distance varied by plant organ and chemical class.Our results describe patterns of specialized metabolite diversity across organs and species and provide support for organ‐specific contributions to plant chemodiversity. This study contributes to the growing understanding within plant evolutionary ecology of the biological scales of specialized metabolite diversification. Future studies combining our data on specialized metabolite diversity with biotic interaction data and experiments can test existing hypotheses on the roles of ecological interactions in the evolution of chemodiversity.
more »
« less
On the mechanical origins of waving, coiling and skewing in Arabidopsis thaliana roots
By masterfully balancing directed growth and passive mechanics, plant roots are remarkably capable of navigating complex heterogeneous environments to find resources. Here, we present a theoretical and numerical framework which allows us to interrogate and simulate the mechanical impact of solid interfaces on the growth pattern of plant organs. We focus on the well-known waving, coiling, and skewing patterns exhibited by roots ofArabidopsis thalianawhen grown on inclined surfaces, serving as a minimal model of the intricate interplay with solid substrates. By modeling growing slender organs as Cosserat rods that mechanically interact with the environment, our simulations verify hypotheses of waving and coiling arising from the combination of active gravitropism and passive root-plane responses. Skewing is instead related to intrinsic twist due to cell file rotation. Numerical investigations are outfitted with an analytical framework that consistently relates transitions between straight, waving, coiling, and skewing patterns with substrate tilt angle. Simulations are found to corroborate theory and recapitulate a host of reported experimental observations, thus providing a systematic approach for studying in silico plant organs behavior in relation to their environment.
more »
« less
- Award ID(s):
- 2209322
- PAR ID:
- 10543200
- Publisher / Repository:
- PNAS
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 121
- Issue:
- 11
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Beneficial rhizobacteria promote plant growth and protect plants against phytopathogens. Effective colonization on plant roots is critical for the rhizobacteria to exert beneficial activities. How bacteria migrate swiftly in the soil of semisolid or solid nature remains unclear. Here we report that sucrose, a disaccharide ubiquitously deployed by photosynthetic plants for fixed carbon transport and storage, and abundantly secreted from plant roots, promotes solid surface motility (SSM) and root colonization by Bacillus subtilis through a previously uncharacterized mechanism. Sucrose induces robust SSM by triggering a signaling cascade, first through extracellular synthesis of polymeric levan, which in turn stimulates strong production of surfactin and hyper-flagellation of the cells. B. subtilis poorly colonizes the roots of Arabidopsis thaliana mutants deficient in root-exudation of sucrose, while exogenously added sucrose selectively shapes the rhizomicrobiome associated with the tomato plant roots, promoting specifically bacilli and pseudomonad. We propose that sucrose activates a signaling cascade to trigger SSM and promote rhizosphere colonization by B. subtilis. Our findings also suggest a practicable approach to boost prevalence of beneficial Bacillus species in plant protection.more » « less
-
Abstract Plants allocate biomass to different organs in response to resource variation for maximizing performance, yet we lack a framework that adequately integrates plant responses to the simultaneous variation in above‐ and below‐ground resources. Although traditionally, the optimal partition theory (OPT) has explained patterns of biomass allocation in response to a single limiting resource, it is well‐known that in natural communities multiple resources limit growth. We study trade‐offs involved in plant biomass allocation patterns and their effects on plant growth under variable below‐ and above‐ground resources—light, soil N and P—for seedling communities.We collected information on leaf, stem and root mass fractions for more than 1,900 seedlings of 97 species paired with growth data and local‐scale variation in abiotic resources from a tropical forest in China.We identified two trade‐off axes that define the mass allocation strategies for seedlings—allocation to photosynthetic versus non‐photosynthetic tissues and allocation to roots over stems—that responded to the variation in soil P and N and light. Yet, the allocation patterns did not always follow predictions of OPT in which plants should allocate biomass to the organ that acquires the most limiting resource. Limited soil N resulted in high allocation to leaves at the expense of non‐photosynthetic tissues, while the opposite trend was found in response to limited soil P. Also, co‐limitation in above‐ and below‐ground resources (light and soil P) led to mass allocation to stems at the expense of roots. Finally, we found that growth increased under high‐light availability and soil P for seedlings that invested more in photosynthetic over non‐photosynthetic tissues or/and that allocated mass to roots at the expense of stem.Synthesis. Biomass allocation patterns to above‐ and below‐ground tissues are described by two independent trade‐offs that allow plants to have divergent allocation strategies (e.g. high root allocation at the expense of stem or high leaf allocation at the expense of allocation to non‐photosynthetic tissues) and enhance growth under different limiting resources. Identifying the trade‐offs driving biomass allocation is important to disentangle plant responses to the simultaneous variation in resources in diverse forest communities.more » « less
-
null (Ed.)Microbiomes from maize and soybean were characterized in a long-term three-crop rotation research site, under four different land management strategies, to begin unraveling the effects of common farming practices on microbial communities. The fungal and bacterial communities of leaves, stems, and roots in host species were characterized across the growing season using amplicon sequencing and compared with the results of a similar study on wheat. Communities differed across hosts and among plant growth stages and organs, and these effects were most pronounced in the bacterial communities of the wheat and maize phyllosphere. Roots consistently showed the highest number of bacterial operational taxonomic units compared with aboveground organs, whereas the α-diversity of fungi was similar between above- and belowground organs. Network analyses identified putatively influential members of the microbial communities of the three host plant species. The fungal taxa specific to roots, stems, or leaves were examined to determine whether the specificity reflected their life histories based on previous studies. The analysis suggests that fungal spore traits are drivers of organ specificity in the fungal community. Identification of influential taxa in the microbial community and understanding how community structure of specific crop organs is formed will provide a critical resource for manipulations of microbial communities. The ability to predict how organ-specific communities are influenced by spore traits will enhance our ability to introduce them sustainably.more » « less
-
ABSTRACT Plant roots shape the rhizosphere community by secreting compounds that recruit diverse bacteria. Colonization of various plant roots by the motile alphaproteobacterium Azospirillum brasilens e causes increased plant growth, root volume, and crop yield. Bacterial chemotaxis in this and other motile soil bacteria is critical for competitive colonization of the root surfaces. The role of chemotaxis in root surface colonization has previously been established by endpoint analyses of bacterial colonization levels detected a few hours to days after inoculation. More recently, microfluidic devices have been used to study plant-microbe interactions, but these devices are size limited. Here, we use a novel slide-in chamber that allows real-time monitoring of plant-microbe interactions using agriculturally relevant seedlings to characterize how bacterial chemotaxis mediates plant root surface colonization during the association of A. brasilens e with Triticum aestivum (wheat) and Medicago sativa (alfalfa) seedlings. We track A. brasilense accumulation in the rhizosphere and on the root surfaces of wheat and alfalfa. A. brasilense motile cells display distinct chemotaxis behaviors in different regions of the roots, including attractant and repellent responses that ultimately drive surface colonization patterns. We also combine these observations with real-time analyses of behaviors of wild-type and mutant strains to link chemotaxis responses to distinct chemicals identified in root exudates to specific chemoreceptors that together explain the chemotactic response of motile cells in different regions of the roots. Furthermore, the bacterial second messenger c-di-GMP modulates these chemotaxis responses. Together, these findings illustrate dynamic bacterial chemotaxis responses to rhizosphere gradients that guide root surface colonization. IMPORTANCE Plant root exudates play critical roles in shaping rhizosphere microbial communities, and the ability of motile bacteria to respond to these gradients mediates competitive colonization of root surfaces. Root exudates are complex chemical mixtures that are spatially and temporally dynamic. Identifying the exact chemical(s) that mediates the recruitment of soil bacteria to specific regions of the roots is thus challenging. Here, we connect patterns of bacterial chemotaxis responses and sensing by chemoreceptors to chemicals found in root exudate gradients and identify key chemical signals that shape root surface colonization in different plants and regions of the roots.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2312761121
