Source: VIRGINIA POLYTECHNIC INSTITUTE submitted to NRP
DISSECTING THE PHYSIOLOGICAL MECHANISMS OF PLANT NUTRIENT RESPONSES TO RISING ATMOSPHERIC CARBON DIOXIDE LEVELS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1031907
Grant No.
2022-67013-42002
Cumulative Award Amt.
$504,028.62
Proposal No.
2023-11870
Multistate No.
(N/A)
Project Start Date
Sep 1, 2023
Project End Date
Oct 31, 2026
Grant Year
2024
Program Code
[A1152]- Physiology of Agricultural Plants
Recipient Organization
VIRGINIA POLYTECHNIC INSTITUTE
(N/A)
BLACKSBURG,VA 24061
Performing Department
(N/A)
Non Technical Summary
The unprecedented rise in atmospheric CO2 concentration ([CO2]) is expected to increase the yields of C3 crops but at the cost of important mineral nutrients. Despite the large body of literature documenting the experimental effects of elevated [CO2] on biomass and nutrient accumulation, the physiological mechanisms that link the increased biomass response with alterations in mineral nutritional content have not been empirically tested. In soybean (Glycine max L. Merr.), there is significant phenotypic variation for biomass and mineral content responses to elevated [CO2] that can be used to dissect the underlying mechanisms of trait responses to rising [CO2]. Eight cultivars of soybean will be utilized in this proposal to answer three research aims: (1) empirically test the hypothesized physiological and molecular mechanisms of mineral composition response to elevated [CO2]; (2) build mathematical models of the underlying physiology of elemental accumulation to test how elevated [CO2] alters elemental accumulation in plants; and (3) validate outputs of these models in a field setting to determine the most likely mechanism(s) associated with lower mineral nutrients in plants in elevated [CO2]. Outputs from growth chamber and field experiments will be used as inputs to build models of the underlying physiology of elemental accumulation under elevated [CO2]. Outcomes from this proposal can be translated directly into molecular resources to develop more climate-resilient crops.
Animal Health Component
10%
Research Effort Categories
Basic
90%
Applied
10%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2061820102060%
2061820108020%
2061820101020%
Goals / Objectives
The current trend of fossil fuel consumption suggests atmospheric carbon dioxide concentration ([CO2]) will rise to at least 650 ppm by the end of the century. This increase in [CO2] is hypothesized to benefit global food production and help meet the demands of a growing population, as elevated [CO2] increases rates of photosynthesis and water-use efficiency in C3plants through a "fertilization" effect. Experimental and meta-analytic data demonstrate that even though growth is enhanced in plants grown in elevated [CO2], protein content, nitrogen concentrations, and most other nutrients aresignificantly decreased. Despite this large body of literature documenting the experimental effects of elevated [CO2] on biomass and nutrient accumulation, the physiological mechanisms that link the increased biomass response to elevated [CO2] with alterations in mineral nutritional content have not been empirically tested.Several hypotheses that are not mutually exclusive may contribute to lower nutrient content with increased biomass in C3plants grown at elevated [CO2], including1.lower transpiration in leaves,2.down-regulation of photosynthesis,3.altered requirements for minerals due to changes in enzyme/organic complex requirements,4.increased carbohydrate and fiber content that dilutes mineral content in seeds and other ograns,5.inhibition of nitrate assimilation by decreaed photorespiration,6.reduction in mineral absorption by roots and altered root architecture, and7.alteration in expression of mineral transporters. While some of these hypotheses have been tested, these analyses did not address changes in nutrient uptake and structure of roots, nor did they perform anyempirical validationof each hypothesis. It is imperative that these studies be performed to increase our understanding of the mechanisms determining elemental accumulation in seeds and other plant organs under sub-ambient, ambient, and elevated [CO2]. Outcomes from these experiments have the potential to be translated directly into molecular resources and tools to develop more climate-resilient crops.The proposed work will leverage the power of multi-scale modeling and extensive physiological studies to improve fundamental understanding of the mechanisms contributing to lower mineral nutrients in plants in elevated [CO2]. This work will be carried using soybean (Glycine maxL. Merr.) as a model C3plant legume system.This research has three objectives: 1. empirically test the hypothesized physiological and molecular mechanisms of mineral composition response to elevated [CO2]; 2. build mathematical models of the underlying physiology of elemental accumulation to test how elevated [CO2] alters elemental accumulation in plants; and 3. validate outputs of these models in a field setting to determine the most likely mechanism(s) associated with lower mineral nutrients in elevated [CO2] in the field. The multidisciplinary PI team will take advantage of soybean cultivars with contrasting mineral nutrient response to elevated [CO2] and other physiological characteristics to enhance our understanding of the physiological basis of mineral accumulation in plant organs under elevated [CO2].
Project Methods
Aim 1: We will empircally test the potential mechanism(s) associated with decreased nutrient accumulation in plants grown in elevated [CO2]. Plants will be grown in growth chambers in sub-ambient [CO2] (~350 ppm) and elevated [CO2] (650 ppm). Plants will be grown in pots in a 14 h/10 h day/night schedule and 25°C day/21°C night temperature conditions and will be fertilized to ensure nutrient content in the soil is not limiting. A total of six chambers (n = 3) in a randomized complete block design will be used. Plants within each chamber will be rotated every 3 days to minimize chamber effects.Aim 1, Task 1. Test if reduced transpiration or mineral dilution alters nutrient distribution. We will grow four cultivars of soybean in replicated growth chamber experiments in sub-ambient and elevated [CO2]: PI398223, PI567201, Loda and HS93-4118. We will measure rates of transpiration using a mini-lysimeter. We will also sample leaf, root, seed, and xylem sap tissues for ionome analysis at vegetative (V5), full pod (R4), beginning seed (R5), and full seed (R6) stages and seeds at full maturity (R8) as well. We will divide the canopy into three sections (top, middle, and bottom) and analyze the leaf and seed ionome in those three parts. Ionome analysis will include Fe, Zn, and 18 other elements and be analyzed by Co-PI Baxter using an ICP-MS. Photosynthesis and stomatal conductance measurements will be taken using a Portable Photosynthesis System (LI-6800) at midday at the V5-R6 time points. Additionally, carbon isotope discrimination will be measured from the same leaf as gas exchange. We will analyze total nonstructural carbohydrate content (TNC) in leaf and seed tissues at the V5-R6 time points. Finally, total seed weight and aboveground biomass will be determined at maturity. We will also perform tissue sampling for RNA-Seq in order to link gene expression and physiological response to elevated [CO2]. Leaf, seed, and root samples will be collected during vegetative and reproductive stages (V5, R4, R5, and R6). RNA will be isolated from leaf, root, and seed tissue collected. DNA libraries will be synthesized from RNA samples sequenced using the Illumina HiSeq 4000 sequencer. Reads will be filtered for quality and mapped to the Wm82.a2.v1 soybean reference genome assembly to determination of transcript abundance values. Differential gene expression analysis will be done using DESeq2.Aim 1, Task 2. Test if down-regulation of photosynthesis or inhibition of nitrate assimilation by decreased photorespiration limits nutrient uptake in elevated [CO2]. For this task will use two genotypes of soybean: a non-nodulating line of soybean without a symbiotic relationship with rhizobia (Williams82-NN) and the corresponding nodulated line (Williams82). We will grow all genotypes in replicated growth chamberexperiments (n = 3) in sub-ambient and elevated [CO2]. Two plants of each cultivar will be assigned to one of three different nutrient treatments corresponding with different nitrogen sources (soil collected at the SoyFACE facility in Illinois (Treatiment 1), Long Ashton solution substituting for the N source with 1 mM NH4Cl (Treatment 2) and 1 mM KNO3 (Treatment 3). We will assess photosynthesis and stomatal conductance and transpiration using the same methods and same time points (V5-R6) as in Aim 1, Task 1. Additionally, A-Ci curves will test whether the different cultivars grown under different nitrogenregimes acclimate to elevated CO2. Leaf and seed tissues will also be sampled for ionomic and TNC analysis using the same methodology as in Aim 1, Task 1. We will only sample at one position in the canopy for ionomic analysis depending on the results in Aim 1, Task 1. Total nitrogencontent and free nitrate will be calculated from the aboveground biomass, and we will use the natural abundance method utilizing 15N isotopic analysis.Aim 1, Task 3. Test if altered requirements for minerals or changes in root architecture/root mineral transport are linked with decreased mineral content in elevated [CO2]. Clark, Flyer, Williams, and Spencer will be grown in replicated GC experiments (n = 3) in sub-ambient and elevated [CO2]. We will perform A-Ci curve analysis as in Aim 1, Task 2. The root structure, ionome, and transcriptome will also be sampled. Root tissue will also be analyzed using a bench top scanner and software (WinRHIZO). Aboveground biomass and total seed weight will also be collected.Aim 2: For the modeling work, we will focus on the critical nutrients, Fe and Zn, although the approach can be easily scaled for other nutrients. We will use a series of systems models with increasing complexity to evaluate the physiological data generated iin Aim 1 for their ability to explain the variation in Fe/Zn and other mineral accumulation in seeds. We will use approximate Bayesian computation to infer parameter values for the underlying processes and identify areas of low sensitivity (more information needed) or high sensitivity (high model confidence/ identifiability). By using genotypes that contrast in their physiological response to elevated [CO2] , we will be able to explore the parameter space of the models more fully. The models will be fit to each genotype and [CO2] separately, and then the parameters and fitting statistics will be compared across genotypes to evaluate how well each model is performing. The models consist of tissue compartments that describe elemental storage dynamics as a function of plant growth. Since little is known about this system, we propose to start with the simplest possible model based on models of root-shoot interactions and resource allocation and uptake. The model has two compartments that increase in size (root, shoot), and two sub-compartments that increase in number and size as the plant grows (trifoliate node sub-compartments, which include seed and leaf). This model will utilize all of the data collected during Aim 1. From the linked genotype and phenotypic analyses, we can begin to distinguish among hypotheses 1-7 by comparing with the predicted model parameters from this aim.Aim 3: We will test the most likely mechanism(s) associated with lower mineral nutrients in elevated [CO2] in the field using the SoyFACE facility in Illinois. We will be grow replicated plots of soybean at ambient [CO2] (~410 ppm) and elevated [CO2] (650 ppm). We will grow all eight cultivars plus Williams82-NN with contrasting phenotypes in the field and assess transpiration rate, down-regulation of photosynthesis, and plant mineral content to determine a link between transpiration rate and/or mineral dilution on seed mineral nutrient concentration and assess the possibility of down-regulation on photosynthesis and altered requirements for minerals on seed mineral concentration in elevated [CO2]. To assess down-regulation of photosynthesis, A-Ci curves will be performed as described in Aim 1, Task 2. We will also sample leaves, seeds, xylem sap, and roots for ionome analysis. We will analyze TNC in leaf and seed tissues as in Aim 1, Task 1. We will also perform tissue sampling for RNA-Seq in order to link gene expression and physiological response to elevated [CO2]. In addition to ionome and RNA sampling in the roots, we will also use a "shovelomic" approach to determine if changes in root architecture occur in plants grown under elevated [CO2]. We will calculate the amount of assimilated nitrogenby analyzing total nitrogencontent and free nitrate, as well as fixed nitrogen from aboveground biomass as in Aim 1, Task 2. Yield will be recorded at R8. Total aboveground biomass will be weighed, and seeds will be threshed with a belt thresher and then weighed. These data will be used to calculate yield and harvest index.

Progress 09/01/23 to 08/31/24

Outputs
Target Audience:There are several target audiences that are the focus of effort for the duration of this USDA NIFA Project. They include: Early Career Researchers: This project reaches early career researchers through both teaching and research mentoring. Undergraduate and graduate students, and a postdoctoral researcher have been served by this project through direct involvement in research projects, data analysis and presentation of their research findings. PI Leisner has advised one graduate student and one undergraduate student, while PI Baxter has advised a postdoctoral researcher at Danforth. PI Sanz has advised one graduate student and several undergraduate researchers at Auburn. Undergraduate and graduate students are also be served by this project through formal teaching at Auburn University through the "Principles of Plant Nutrition" course and "Crop Physiology" course taught annually by PI Sanz and the "Plant Genomics and Stress" course taught by PI Leisner at Virginia Tech. Breeders: Through collaboration with the soybean breeders at Auburn University in the Crop, Soil and Environmental Science department and the School of Plant and Environmental Sciences at Virginia Tech we will work to directly translate the research findings in a way that will facilitate future breeding efforts focused on climate change resilience. Broader scientific community: The findings from this work will be disseminated through conference presentations and open-access peer-reviewed publications. Additionally, data will be deposited in public repositories (NCBI and Github). This will allow the larger scientific community access to our research findings and increase understanding and awareness of climate change impacts on plant nutritional quality. Changes/Problems:We had issues with proper CO2fumigation of our growth chambers during the growth chamber experiment testing hypotheses 1 and 4 (Aim 1-Task 1). Due to the fumigation issues, we only have a single biological replicated for the elevated CO2treatment. We are now repeating this growth chamber experiment at Virginia Tech. We also encountered issues hiring a postdoctoral researcher on the project due to visa issues however, we have worked around this now and are completing the work with two graduate students. The second graduate student with PI Sanz started in January 2024. Finally, PI Leisner has moved her research group from Auburn University to Virginia Tech (VT). The graduate student working with Dr. Leisner also moved with the lab. This has ensured a smooth transition of the project, however there was a pause in data collection and analysis while the lab was transitioning during summer 2023. The wet lab is now set-up for PI Leisner at VT, and she has also access to more growth chambers with CO2fumigation. This will facilitate simultaneous replication of the growth chamber at VT and Auburn and increase the ability to complete all growth chamber experiments in the next reporting period. What opportunities for training and professional development has the project provided?Through the role of the PIs at Virginia Tech, Auburn University and the Donald Danforth Plant Science Center, we have provided teaching and mentoring to the students and postdoc involved in the project. As mentors (Leisner, Sanz-Saez and Baxter) we have provided them with the skills and learning environment to further their own curiosity and research endeavors in climate change impacts on food production. PIs Leisner and Sanz-Saez also teach courses focused on plant physiology and climate change which will are open to upper-level undergraduate students and graduate students at their respective universities. Additionally, all PIs and the Collaborator (Ainsworth) meet monthly to discuss project goals, recent progress, project hurdles and next steps. This gives graduate students and the postdoc on the project and opportunity to network with all PIs on the proposal and practice their scientific communication skills. We also had an in-person project meeting following the Crop Science Society of America meeting in St. Louis, Missouri on October 31st, 2023. This was hosted by PI Baxter at the Danforth Center. All PIs (Baxter, Leisner, Sanz) and collaborators (Ainsworth) participated, along with all graduate students in each lab who participate on the project. Additionally, the postdoctoral researcher advised by PI Baxter was in attendance. The goals of this project meeting were: 1) provide in-person networking opportunities for all members of the project; 2) give early career researchers an opportunity to practice presenting their scientific research; 3) discuss new or additional analyses that can be done with the data in hand, and; 4) focus on how we can use the current physiological data to enhance the modeling component of our proposal (Aim 2). How have the results been disseminated to communities of interest?All data produced from this proposal will be publicly available through use of data servers after publication, data repositories (i.e., GitHub) and federal data repositories (NCBI and SRA). Funds from this project will continue to be used to provide open access to all future publications to make them freely available to the public. The two publications already resulting from this proposal are open-access. The research conducted under this project (completed by the PIs, undergraduates, graduate students, and postdocs) was presented at the Crop Science Society meeting St. Louis, Missouri in October 2023. Dissecting the Physiological Mechanisms of Plant Nutrient Responses to Rising Atmospheric Carbon Dioxide Levels.Courtney Leisner,Mary Durstock, Ravneet Kaur, Elizabeth A Ainsworth, Ivan Baxter and Alvaro Sanz-Saez. Soybean in an Elevated CO2World: Utilizing Transcriptomic Analyses to Identify the Physiological Mechanisms Linking Increased Biomass and Altered Mineral Nutrition.Ravneet Kaur, Mary Durstock, Renee Dale, Elizabeth A Ainsworth, Ivan Baxter, Alvaro Sanz-Saez, and Courtney Leisner. What do you plan to do during the next reporting period to accomplish the goals?The last large-scale growth chamber experiment to analyze the hypothesized mechanisms of elevated CO2on nutrient content (Aim 1-Task 3) will begin in January 2025. We will complete all growth chamber experiments associated with Aim 1, which addresses objective 1 of our proposal. Additionally, we will continue working on building the mathematical model of how elevated CO2affects nutrient accumulation in soybean (Aim 2). In summer of 2025 we will grow all 8 cultivars of soybean at the SoyFACE facility with Collaborator Ainsworth. This will help usvalidate outputs of the growth chamber experiments and mathematical models in a field setting to determine the most likely mechanism(s) associated with lower mineral nutrients in elevated [CO2] in the field (Aim 3). We will continue monthly meetings and work on a peer-reviewed manuscript from data generated in Year 1 and 2. Additionally, the data from this work will be presented at the American Society of Plant Biology meeting and summer 2025.

Impacts
What was accomplished under these goals? Data collected in Year 1 is currently being analyzed. First, we have data from an open-top chamber experiment to analyze elevated CO2impacts on physiology, transcript expression and nutrient content in 3 cultivars of soybean (Clark, Flyer, and Loda). The physiology data from the OTC chamber experiment is currently under review atPlant Physiology(see list of publications in previous section, Kaur et al., 2024). For the transcriptomic data we are analyzing differentially expressed genes across the 3 soybean cultivars in 3 tissues (leaves, pods, and roots). One graduate student is currently finalizing gene coexpression analysis and this data will be submitted for publication by the end of 2024. Additionally, we are analyzing data from a completed pilot growth chamber experiment with 8 cultivars of soybean to test the controlled growth chamber CO2fumigation and test all methods related to physiological impacts on nutrition in soybean as outlined in the proposal. We also completed a new growth chamber experiment in Year 2. This experiment was Aim 1-Task 1 of our proposal which focused on analyzing hypotheses 1 and 4. We grew 4 cultivars of soybean under sub-ambient and elevated CO2concentrations and took physiological and yield measurements during several key developmental time points (V5, R5 and R8). Due to issues with our CO2 fumigation in the chamber we are now in the process of doing this growth chamber experiment again. The plants are close to R5 (full pod) and the experiment will be completed when plants reach maturity (R8). PI Sanz has completed the growth chamber experiment proposed in Aim 1-Task 2 to test if down-regulation of photosynthesis or inhibition of nitrate assimilation by decreased photorespiration limits nutrient uptake in elevated CO2conditions. PI Sanz is working with a graduate student to analyze this data and will begin a replication of this experiment in Fall 2024. PI Sanz is also working with this graduate student to quantify root characteristics and root hair abundance across cultivars to determine if root characteristics and root hair abundance is a possible mechanism associated with changes in nutrient uptake in elevated[CO2]. PI Baxter has been working with a postdoctoral researcher tobuild a mathematical model of the underlying physiology of elemental accumulation to test how elevated [CO2] alters elemental accumulation in plants. This work is also done in collaboration with PI Sanz, PI Leisner and their respective graduate students. We currently have a preliminary mathematical model that we are working to refine.?

Publications

  • Type: Journal Articles Status: Published Year Published: 2024 Citation: Digrado, A., Montes, C. M., Baxter, I., & Ainsworth, E. A. (2024). Seed quality under elevated CO2 differs in soybean cultivars with contrasting yield responses. Global Change Biology, 30(2), e17170.
  • Type: Journal Articles Status: Under Review Year Published: 2024 Citation: Kaur, R. et al. Nutrient Challenges in a Changing Atmosphere: Investigating Biomass Growth and Mineral Concentration Changes in Soybean Plants under Elevated CO2. bioRxiv 2024.08.02.606357 (2024) doi:10.1101/2024.08.02.606357.