Source: PENNSYLVANIA STATE UNIVERSITY submitted to
ROOT TRAITS FOR BETTER CROP PERFORMANCE UNDER ABIOTIC STRESS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
1005492
Grant No.
(N/A)
Project No.
PEN04582
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Jan 1, 2015
Project End Date
Dec 31, 2019
Grant Year
(N/A)
Project Director
Brown, KA, MA.
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802
Performing Department
Plant Science
Non Technical Summary
Drought and low soil fertility are major limitations to worldwide crop production. In poor nations, these constraints depress yields to only a fraction of yield potential, causing poverty and food insecurity, while in rich nations, intensive fertilization is the largest economic, energy, and environmental cost of grain production, while drought is the greatest risk. Abiotic stress is projected to become more severe in coming decades as a result of global climate change and accelerating degradation of soil and water resources. The development of crops with greater tolerance to abiotic stress is therefore an urgent priority.Past breeding for stress-tolerant crops has relied primarily on yield trials, which are imprecise, costly, and sample a limited range of environments and management options. Recent developments in crop physiology, phenomics, genomics, and technology dissemination present opportunities to accelerate breeding progress by targeting specific traits and integrating them into breeding programs via marker-assisted breeding, trait phenotyping, and trait-based selection.The development of stress tolerant crops will be greatly facilitated by 1) the identification of specific traits improving yield under stress 2) understanding the genetic control of these traits, and 3) development of phenotyping platforms to rapidly screen crop germplasm for these traits, to support gene discovery as well as direct phenotypic selection. Our project will develop basic information and technical resources to enable utilization of beneficial root traits in crop breeding programs to improve crop yields under drought and low soil fertility.
Animal Health Component
0%
Research Effort Categories
Basic
20%
Applied
60%
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2031410102025%
1021510107015%
2031510102020%
2011510108010%
2011410108010%
2011530108010%
2062420102010%
Goals / Objectives
To assess the value of root traits in specific stress environments via empirical studies and modeling.Identification of the genetic basis for root traits.Determination of the agroecological impacts of trait deployment.
Project Methods
Experiments will be conducted using publically available germplasm, including diversity panels assembled for genome-wide association studies to determine the genetic control of root traits in crops. Plants will be grown in various environments depending on the purpose of the experiments. Plants will be grown in the laboratory for detailed studies of seedling architecture and behavior and for kinetic and kinematic studies of root growth. Plants will be grown in the greenhouse for studies of detailed physiological and growth responses to nutrient and drought sstress. Field studies will be used to test the value of specific traits under drought and nutrient stress and their impact on yield. Simulation modeling using the structural-functional model SimRoot will be used to test trait combination scenarios. Experiments will be analyzed using standard statistical methods. Genetic information in mapping studies will be analysed using specialized statistical techniques designed for that purpose, such as Gapit. Results will be published in appropriate venues and disseminated to collaborators, including plant breeders, for utilization in breeding programs.

Progress 01/01/15 to 12/31/19

Outputs
Target Audience:The primary target audiences are public and private sector plant breeders and breeding organizations interestedin developing new cultivars with improved tolerance to soil stresses. Our research provides information about root phenotypes that are useful in various stress environments and their agronomic tradeoffs. In addition, we conduct genetic analyses that permit the use of marker assisted selection of these traits for cultivar development. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project included training of eight Ph.D. students and one M.S. student, six post-doctoral researchers, two undergraduate students, and two visiting scholars (one from Thailand and one from Denmark) during the current reporting period. The postdoctoral scholars and graduate students took advantage of numerous professional training opportunities, including local, national, and international presentations of their research. One undergraduate student conducted research both at Penn State and with our partner institution the University of Nottingham, UK, on a related project. How have the results been disseminated to communities of interest?In addition to scientific publications, which are available to those in seed-related industries, our team has presented the results of this project to various audiences via seminars and workshops. PI Lynch presented 10 seminars, two of which were international, with overviews of our major projects. PI Brown presented a seminar in a workshop of the American Phytopathological Society oriented toward engaging disparate groups of researchers interested in root-rhizosphere microbiome interactions. PI Duque presented two talks at national fora for sweetpotato researchers, an international talk and poster for researchers of tropical crops, and a local seminar. Postdoctoral scholar Burridge presented a seminar at LANGBIO-CINVESTAV Mexico on our work on climate resilient beans, and also participated in an event in Mozambique celebrating the release of new bean cultivars there. Postdoctoral scholar Hanlon presented research on X-ray fluorescence to determine root depth from leaf elemental signatures at the Phenome meeting in Arizona.Postdoctoral scholar Schneider presented anatomics research in a seminar at the University of Nottingham. Two of our graduate students presented workshops for high school students attending the Governor's School summer program at Penn State and for incoming freshman scholars at Penn State. Another graduate student presented a workshop for Penn State undergraduate students interested in international agriculture. Another graduate student presented two seminars at the rice department research locations in Bangkok and Ubon Thailand. PI Lynch presented a workshop to graduate students at the University of Nottingham on our "shovelomics" method of root system excavation and analysis. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Goal 1. Roots are complex organs composed of many different traits, which vary among genotypes and can change in response to soil conditions, such as fertility, water availability and compaction. We have developed methods to investigate these traits, including breaking down traits into individual components called phenes, developing new methods to define and measure various root structures at different scales, and evaluating genetic variation and plasticity of traits, i.e. how they change in response to soil conditions. To complement previous methods to evaluate root architecture, we developed a new high-throughput method to evaluate root anatomy based on imaging root tissues as they are vaporized by a laser, called laser ablation tomography (LAT). This system allows evaluation of the cellular features of roots that influence the cost of the root in terms of carbohydrate and nutrients, as well as the ability of the root to take up water and nutrients, penetrate through hard soil, and to resist pathogens and herbivores. This system was used to investigate how previously known and novel root anatomical traits can affect plant performance under stressful soil conditions. These traits, along with root architectural traits, such as numbers, angles, and lengths of roots in various classes, were tested in lab, greenhouse, and field conditions in the United States and abroad to demonstrate their value for increasing crop resilience and productivity. Over the course of this project, we have investigated root traits of several annual crop species. One focus has been Phaseolus vulgaris (common bean), an important food security crop in Latin America and Sub-Saharan Africa, as well as a vegetable crop in the United States. Root traits of common bean were compared with those of related legumes, including species that are more drought tolerant, and ideotypes (ideal trait combinations) were developed to guide breeding programs, taking advantage of strategies already employed by crop relatives. Similar approaches were taken with maize and related species such as sorghum, maize landraces, and teosinte (maize ancestors). The value of selected strategies has also been tested in other grasses such as barley and rice. For example, we showed that more aerenchyma (air spaces in the root cortex) and fewer, larger cortical cells reduce the metabolic cost per unit root length in maize. The same goal is accomplished via increased root cortical senescence in barley, while common bean reduces secondary growth and continues to elongate thinner roots. Optimal root branching strategies depend on the type of soil stress. Denser, shallow branching of many axial roots is better for low phosphorus soils, while sparser lateral root branching with greater elongation of fewer axial roots results in deeper root distribution to capture nitrogen and water in drought and nitrogen leaching scenarios. A new storage root phenotyping platform was developed using an expandable ebb and flow greenhouse production and imaging system. Genetic and low phosphorus-induced variation was demonstrated for sweetpotato root architectural and anatomical traits and starch accumulation. Root traits and phenes interact with each other and may produce positive or negative synergies. While some trait combinations were explored experimentally, a much greater number can be explored in silico using our structural-functional root model OpenSimRoot. OpenSimRoot was expanded from the previous version to permit testing of various root trait combinations for rice and sorghum in addition to the previous species maize and common bean, and under drought and impedance (soil compaction) stresses were added to the previously available nutrient stress capabilities. Goal 2. We have evaluated large panels of germplasm for maize, several legumes, and cultivated rice to identify genetic regions responsible for natural variation in various root traits. Genetic markers were reported for several root architectural traits of cowpea (Vigna unguiculata), and one trait, basal root angle, was correlated with tolerance to the parasitic weed Striga gesnerioides. Genomic regions associated with a large number of root architectural and anatomical traits have been identified in maize, common bean, and rice. Goal 3. Roots interact intimately with soil and compete for soil resources with other roots from the same and different plants and with soil organisms. Increases in planting density in maize over the past century have led to inadvertent selection for roots with slightly fewer nodal roots with shallower angles, which better tolerate competition, especially for nitrogen. Simulations and empirical studies have indicated that increasing aerenchyma would be valuable for maize under drought and nutrient stress, but we also showed that greater aerenchyma is associated with changes to the soil microbiome, particularly in a sandy soil with low organic matter, where the oxygenation capability of aerenchyma enriched species with aerobic metabolism and those postulated to be involved in nitrogen transformations, including the ammonia oxidizing family Nitrososphaeraceae. In a clay soil with more nitrogen and organic matter, bacteria in the Xanthomonadaceae family were enriched. This family is associated with disease-suppressive soils and pathogen antagonists. In another study, we found that root anatomical traits affected root Fusarium disease incidence and mycorrhizal colonization in maize grown in agricultural soils in Pennsylvania. Nodal roots of hybrid maize plants with few, large cortical cells were also less likely to harbor Fusarium infections, while plants with more aerenchyma had more mycorrhizal colonization. Thus, anatomical phenotypes previously associated with greater metabolic efficiency had benefits for biotic associations in the field.

Publications

  • Type: Journal Articles Status: Awaiting Publication Year Published: 2019 Citation: Burridge JD, Findeis, Jill L, Jochua, Celestina, N, Mubichi-Kut, Fridah, M, Miguel, Magalhaes A., Quinhentos, Maria L., Xerinda, Soares A., Lynch, Jonathan, P (2019) A case study on the efficacy of root phenotypic selection for edaphic stress tolerance in low-input agriculture: common bean breeding in Mozambique. Field Crops Research, in press.
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2019 Citation: Lorts, C, Lynch JP, Brown KM (2019) Parental effects and provisioning under drought and low phosphorus stress in common bean. Food and Energy Security, in press.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Galindo-Casta�eda T, Brown KM, Kuldau GA, Roth GW, Wenner NG, Ray S, Schneider H, Lynch JP (2019) Root cortical anatomy is associated with differential pathogenic and symbiotic fungal colonization in maize. Plant Cell Environ. doi: 10.1111/pce.13615
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Hall B, Lanba A, Lynch J (2019) Three-dimensional analysis of biological systems via a novel laser ablation technique. J Laser Appl 31: 22602
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Hazman M, Brown KM (2018) Progressive drought alters architectural and anatomical traits of rice roots. Rice 11: 62
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Lynch JP (2019) Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytol 223: 548564
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Le Mari� CA, York LM, Strigens A, Malosetti M, Camp K-H, Giuliani S, Lynch JP, Hund A (2019) Shovelomics root traits assessed on the EURoot maize panel are highly heritable across environments but show low genotype-by-nitrogen interaction. Euphytica 215: 173
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Oladzad A, Porch T, Rosas JC, Moghaddam SM, Beaver J, Beebe SE, Burridge J, Jochua CN, Miguel MA, Miklas PN, et al (2019) Single and Multi-trait GWAS Identify Genetic Factors Associated with Production Traits in Common Bean Under Abiotic Stress Environments. G3 Genes|Genomes|Genetics 9: 1881 LP  1892
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Strock CF, Burridge J, Massas ASF, Beaver J, Beebe S, Camilo SA, Fourie D, Jochua C, Miguel M, Miklas PN, et al (2019a) Seedling root architecture and its relationship with seed yield across diverse environments in Phaseolus vulgaris. F Crop Res 237: 5364
  • Type: Theses/Dissertations Status: Submitted Year Published: 2019 Citation: Strock CF 2019 Functional implications of root architectural and anatomical phenes for soil resource capture. Ph.D. Plant Biology, Penn State University.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Duque LO, Villordon A. 2019. Root Branching and Nutrient Efficiency: Status and Way Forward in Root and Tuber Crops, Front. Plant Sci. 10:237
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Strock CF, Schneider HM, Galindo-Casta�eda T, Hall BT, Van Gansbeke B, Mather DE, Roth MG, Chilvers MI, Guo X, Brown K, Lynch JP (2019b) Laser Ablation Tomography for Visualization of Root Colonization by Edaphic Organisms. J Exp Bot 70: 53275342
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Yang JT, Schneider HM, Brown KM, Lynch JP (2019) Genotypic variation and nitrogen stress effects on root anatomy in maize are node specific. J Exp Bot 70: 53115325


Progress 10/01/17 to 09/30/18

Outputs
Target Audience:The research in this project is designed to develop tools to enable breeding of crops that are more resilient to soil stresses. These tools would be used by other researchers interested in crop adaptation and improvement, and by public and private plant breeders who could use the tools to select for better adaptation to their target environments. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project included training for 15 graduate students, four postdoctoral researchers, seven visiting scholars, and six undergraduate students. Professional opportunities included: two graduate students attended and participated in the Gordon Conference on Salt and Water Stress in New Hampshire, two students and two postdoctoral researchers attended and presented posters at the American Society of Plant Biologists meeting in Montreal, one postdoctoral researcher organized and presented multiple talks at a USAID project meeting in Cali, Colombia, another postdoctoral researcher organized and presented a talk at a team meeting of our ARPA-e project at Penn State. She also attended and presented team progress at the annual ARPA-e ROOTS program meeting in San Francisco, visited collaborator groups at Colorado State University and the University of Wisconsin to plan and conduct experiments at those sites, and presented a poster at the conference "Big Data Driven Agriculture" in Washington DC. Another postdoctoral researcher attended and presented a talk at the Plant Genomics and Gene Editing Congress in Philadelphia. A graduate student attended and presented a poster at the Joint International Sweet Corn Development Association and the Corn Breeding Research Annual Meeting. One student and one postdoctoral researcher attending a training session for the Li-Cor infrared gas analyzer, used for photosynthesis and respiration measurements. Undergraduate students presented their research at on-campus research exhibitions. How have the results been disseminated to communities of interest?Results of our work have been made available through scientific peer-reviewed publications and by presentations at universities and conferences. As listed in the previous section, our graduate students and postdoctoral researchers have been active in presenting their research at conferences and engaging in collaborative research projects with other institutions domestically and internationally. The PIs and postdoctoral researchers have presented invited talks at several universities, one major agricultural corporation, at conferences in the US, UK, France and Sweden, and at collaborative research project meetings in the US, UK, Colombia, and Thailand. The collaborative projects include researchers and plant breeders. New seed developed under USAID funding of the legume innovation lab is distributed through governmental organizations in Mozambique, and in the Caribbean by seed companies and governmental organizations. What do you plan to do during the next reporting period to accomplish the goals?Results of genome-wide association studies in maize, bean and rice will be analyzed and reported as scientific papers. Some of the genetic associations will be examined further and confirmed with additional experiments in collaboration with project partners. We will continue to explore root phenes and phene combinations for better performance under edaphic stress.

Impacts
What was accomplished under these goals? Goal 1. To assess the value of root traits in specific stress environments via empirical studies and modeling. Efficient root systems are characterized by reduced cost per unit root length and increased acquisition of nutrients and water per unit investment of carbon or the limiting nutrient in the root system. Plants typically allocate resources to the root system that can be divided among root classes, and branching vs. elongation, in various ways. What is optimal for a root system depends on the specific environment. For example, we previously showed that maize plants with fewer crown roots produced deeper roots and had improved acquisition of water under drought stress, where water is typically available in deeper soil layers. Now we have shown that the opposite phenotype is more valuable under low phosphorus stress, i.e. a larger number of crown roots improves topsoil exploration and allows the plant to acquire more of that shallow resource. Similarly, fewer but longer lateral roots promoted better performance under drought, but a larger number of shorter lateral roots promoted better performance under low phosphorus stress. Since nitrogen leaches into the deeper soil layers over time, we expect phenotypes that are valuable for drought and low nitrogen to be similar. When both shallow and deep resources are limiting, e.g. the plant is grown with both low phosphorus and low nitrogen or drought, co-optimization of root traits is needed. Using the structural-functional model SimRoot, we investigated combinations various values for basal root whorl number (functionally similar to crown root number in maize) basal root growth angles, and lateral root branching density for the performance of common bean under combined nitrogen and phosphorus stress. The value of each phene state depended on the particular stress combination and on other phenes. A phenotype with three whorls of basal roots was optimal for most conditions. This phenotype facilitates good soil exploration without excess carbon cost or intraplant competition. When basal roots expressed a range of angles, i.e. created a fanned shape, the root system demonstrated greater vertical distribution and the ability to acquire both shallow and deep nutrients. Root systems could partially compensate for deeper root distribution with the development of hypocotyl-borne roots, but these were mostly useful for shallow resource acquisition. Goal 2. Identification of the genetic basis for root traits. Root traits are under both genetic and environmental control. We have estimates of heritability of various architectural and anatomical phenes in field-grown maize and bean plants ranging from very low (0.1) to very high (0.86). Root anatomical phenes tended to have greater heritability than root architectural phenes. Many phenes demonstrate significant plasticity, i.e. changes in response to a specific environmental change, in this case nutrient or water stress, and this plasticity also has some degree of genetic control. In a genome-wide association analysis of root traits in a temperate-adapted maize diversity panel (Wisconsin Diversity Panel) grown under irrigated and drought-stress conditions in the field, very few common gene models were associated with root traits under irrigated vs. drought conditions or for either condition and plasticity of the trait. Many genes associated with trait plasticity were associated with abiotic stress ontogenic categories. Goal 3. Determination of the agroecological impacts of trait deployment Root cortical aerenchyma, the development of air spaces in the root cortex, reduces the carbon cost of root maintenance, permitting greater root elongation and resource acquisition. Since there is broad genetic variation for this trait, it is likely that it has a beneficial or harmful effect depending on the environment. Loss of cortical cells during aerenchyma development reduces living cortical area, which is the habitat for arbuscular mycorrhiza colonization. Arbuscular mycorrhiza acquires phosphorus and transfers it to the host plant in exchange for fixed carbon, and is particularly important for crops grown in low phosphorus soils. In maize, there was up to 55% less arbuscular mycorrhiza colonization in genotypes with less living cortical area, but this decrease did not lead to reduced phosphorus acquisition or biomass, probably because lateral roots with less aerenchyma are responsible for the majority of phosphorus acquisition.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Jia X, Liu P, Lynch J (2018) Greater lateral root branching density in maize (Zea mays L.) improves phosphorus acquisition from low phosphorus soil. J Exp Bot 69:49614970.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Galindo-Casta�eda T, Brown KM, Lynch JP (2018) Reduced root cortical burden improves growth and grain yield under low phosphorus availability in maize. Plant Cell Environ 41(7):15791592.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Gage JL, Jarquin D, Romay C, Lorenz A, Buckler ES, Kaeppler S, Alkhalifah N, Bohn M, Campbell DA, Edwards J, Ertl D, Flint-Garcia S, Gardiner J, Good B, Hirsch CN, Holland J, Hooker DC, Knoll J, Kolkman J, Kruger G, Lauter N, Lawrence-Dill C, E Lee, Lynch JP, Murray S, Nelson R, et al. (2017) The effect of artificial selection on phenotypic plasticity in maize. Nat Commun 8(1). doi:10.1038/s41467-017-01450-2.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Strock CF, Morrow de la Riva L, Lynch J (2017) Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition. Plant Physiol. Available at: http://www.plantphysiol.org/content/early/2017/11/08/pp.17.01583.abstract.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Bhosale R, Giri J, Pandey BK, Giehl RFH, Hartmann A, Traini R, Truskina J, Leftley N, Hanlon M, Swarup K, Rashed A, Vo� U, Alonso J, Stepanova A, Yun J, Ljung K, Brown KM, Lynch JP, Dolan L, et al. (2018) A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat Commun 9(1):1409.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Hanlon MT, Ray S, Saengwilai P, Luthe D, Lynch JP, Brown KM (2018) Buffered delivery of phosphate to Arabidopsis alters responses to low phosphate. J Exp Bot 69(5). doi:10.1093/jxb/erx454.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Lynch JP (2018) Rightsizing root phenotypes for drought resistance. J Exp Bot:ery048-ery048.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: AlKhalifah N, Campbell DA, Falcon CM, Gardiner JM, Miller ND, Romay MC, Walls R, Walton R, Yeh C-T, Bohn M, Bubert J, Buckler ES, Ciampitti I, Flint-Garcia S, Gore MA, Graham C, Hirsch C, Holland JB, Hooker D, et al. (2018) Maize Genomes to Fields: 2014 and 2015 field season genotype, phenotype, environment, and inbred ear image datasets. BMC Res Notes 11(1):452.
  • Type: Theses/Dissertations Status: Published Year Published: 2017 Citation: Hanlon M (2017) New perspectives on conventional ideas about root system architecture and morphology. Dissertation (Penn State University).
  • Type: Theses/Dissertations Status: Published Year Published: 2017 Citation: Schneider H (2017) Functional implications of root cortical senescence for soil resource capture. Dissertation (Penn State University).
  • Type: Theses/Dissertations Status: Published Year Published: 2017 Citation: Yang JT (2017) Integrating root and leaf phenotypes to enhance nitrogen use efficiency in maize (Zea mays L.). Dissertation (Penn State University).
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Orman-Ligeza B, Morris EC, Parizot B, Lavigne T, Bab� A, Ligeza A, Klein S, Sturrock C, Xuan W, Nov�k O, Ljung K, Fernandez MA, Rodriguez PL, Dodd IC, De Smet I, Chaumont F, Batoko H, P�rilleux C, Lynch JP, et al. (2018) The Xerobranching Response Represses Lateral Root Formation When Roots Are Not in Contact with Water. Curr Biol 28(19):31653173.e5.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Rangarajan H, Postma J, Lynch J (2018) Co-optimization of axial root phenotypes for nitrogen and phosphorus acquisition in common bean. Ann Bot 122(3):485499.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Schneider HM, Wojciechowski T, Postma JA, Brown KM, Lynch JP (2018) Ethylene modulates root cortical senescence in barley. Ann Bot 122(1):95105.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Schneider HM, Lynch JP (2018) Functional implications of root cortical senescence for soil resource capture. Plant Soil 423(1):1326.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Sun B, Gao Y, Lynch J (2018) Large crown root number improves topsoil foraging and phosphorus acquisition. Plant Physiol 177(May):pp.00234.2018.


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:Our work directly supports the research of graduate students and faculty at Penn State and other institutions interested in root biology and phenomics. The scientific community at large benefits via public presentations of our work at conferences and invited lectures as well as from our publications. Public and private sector plant breeders benefit via our direct interaction on funded projects and from our public presentations and publications. They use our work to guide their selection process during breeding. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project included training for 14 graduate students, one postdoctoral researcher, nine visiting scholars, and six undergraduate students. Professional opportunities included: seven graduate students and a postdoctoral researcher attended the Interdisciplinary Plant Group annual symposium in Root Biology in Columbia MO, and five of them presented posters there. Stephanie Klein and Meredith Hanlon visited the DOE TERRA site at Maricopa AZ to investigate possible research collaboration. Stephanie Klein attended and presented a poster at the Xylem International Meeting in France. She also attended the Workshop of Cereal Genomics at Cold Spring Harbor and visited our collaborator lab (Shawn Kaeppler, Univ. Wisconsin) to learn GWAS techniques. James Burridge, working on a USAID funded project, presented 2 posters at the Pan-African Grain Legume & World Cowpea Conference, conducted collaborative research trials with colleagues at UC Riverside, ARS in Prosser, Washington, and EAP-Zamorano Honduras, and organized a project meeting that included presenting his research at Penn State. Two other graduate students, Anica Massas and Christopher Strock, also presented their research at our USAID project meeting. Jennifer Yang attend the Congressional Visits Day sponsored by the tri-societies (Crop Science, Agronomy, Soil Science). Hannah Schneider presented posters at the Phenome 2017 conference in Arizona and at the 4th international plant phenotyping symposium in Mexico, and participated in a Next-Gen sequencing data analysis workshop in Germany. Meredith Hanlon attended the ARPA-e ROOTS program kickoff meeting in Missouri. How have the results been disseminated to communities of interest?Results of our work have been made available through scientific peer-reviewed publications and by presentations at universities and conferences. As listed in the previous section, our graduate students and postdoctoral researcher have been active in presenting their research at conferences and engaging in collaborative research projects with other institutions domestically and internationally. The PIs have presented invited talks at several universities, at conferences in the US, UK, and Sweden, and at collaborative research project meetings in the US and the Philippines. The collaborative projects include researchers and plant breeders. What do you plan to do during the next reporting period to accomplish the goals?We are starting a new research project funded by DOE ARPAe focused on developing techniques for selection of deeper-rooted maize for improved carbon sequestration, nitrogen capture, and drought tolerance. This will include further development of root traits and breeder-friendly selection methods, a non-destructive method for assessing root depth in the field, and an automated platform for root excavation and imaging. In addition, we will be continuing research on root traits of common bean and rice as related to improved abiotic stress tolerance.

Impacts
What was accomplished under these goals? Goal 1. To assess the value of root traits in specific stress environments via empirical studies and modeling. We assessed the relationship of root architectural and anatomical traits to performance under low nitrogen using maize inbred and hybrid lines. There was genetic variation for the plasticity of root traits in response to low nitrogen stress. Generally, size-related traits showed a negative response to low nitrogen, but there were exceptions. Axial roots altered their anatomical response to low nitrogen depending on the node from which the root originated. Roots arising from the youngest nodes had larger diameters and disproportionate increases in stele areas. Roots from nitrogen-efficient genotypes had less increase in aerenchyma and less decrease in metaxylem number and median area than less efficient genotypes. A negative relationship was found among IBM recombinant inbred lines for nodal root number and nodal root diameter. Genotypes with fewer but thicker nodal roots were found to have better growth under moderate nitrogen stress. The greater cost of thicker nodal roots appeared to have been more than offset by the reduced number of nodal roots, resulting in increased nodal root length that effected greater nitrogen capture from deeper soil. Goal 2. Identification of the genetic basis for root traits. Cowpea (Vigna unguiculata L.) is an important food security crop in Africa, Asia, and South America, and makes important contributions to agroecosystems due to its tolerance of drought and low soil fertility and ability to fix nitrogen. A diversity panel comprised of 189 landraces and elite breeding lines of cowpea was used to investigate the genetic control of root architectural traits. Eleven quantitative trait loci (QTL) were identified, including six that co-located with previously identified QTL for traits related to yield at typical cowpea production sites in Africa. In a separate study, a rice diversity panel was used for a genome-wide association study of root traits including root hairs. Investigation of the candidate genes arising from this study revealed that very few candidates were found in databases of genes and transcripts associated with root hair development in the model plant Arabidopsis, indicating that either (1) dicots and monocots have very different programs of root hair development; or (2) mutant studies used for annotation of genes involved in root hair development do not lead to identification of genetic factors important for natural variation of the trait. One significant association, with root hair density on chromosome 9, was found to result from an introgression from the aus subpopulation into the indica subpopulation, where the aus genotype in the region was associated with denser hairs. Goal 3. Determination of the agroecological impacts of trait deployment. Several QTL identified in the cowpea association mapping study discussed above were also found to be associated with Striga tolerance. Striga (Striga gesneroides) is a parasitic weed that can be devastating in some cowpea production areas. The alleles that were associated with Striga tolerance were root architecture traits conferring deeper roots. We suggest that the tolerance conferred by these QTL is one of avoidance of Striga germination or attachment to the potential host cowpea plant by preferential root growth in deeper soil domains.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Bucksch A, Atta-Boateng A, Azihou AF, et al. 2017. Morphological Plant Modeling: Unleashing Geometric and Topological Potential within the Plant Sciences. Frontiers in Plant Science 8, 900.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Burridge JD, Schneider HM, Huynh B-L, Roberts PA, Bucksch A, Lynch JP. 2017. Genome-wide association mapping and agronomic impact of cowpea root architecture. Theoretical and Applied Genetics 130, 419431.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Marshall-Colon A, Long SP, Allen DK, Allen G, Beard DA, Benes B, von Caemmerer S, Christensen AJ, Cox DJ, Hart JC, Hirst PM, Kannan K, Katz DS, Lynch J, Millar AJ, Panneerselvam B, Price ND, Prusinkiewicz P, Raila D, Shekar RG, Shrivastava S, Shukla D, Srinivasan V, Stitt M, Turk MJ, Voit EO, Wang Y, Yin X, Zhu X 2017. Crops In Silico: Generating Virtual Crops Using an Integrative and Multi-scale Modeling Platform. Frontiers in Plant Science 8, 786.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Postma JA, Kuppe C, Owen MR, Mellor N, Griffiths M, Bennett MJ, Lynch JP, Watt M. 2017. OpenSimRoot: widening the scope and application of root architectural models. New Phytologist 215, 12741286.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Schneider HM, Postma JA, Wojciechowski T, Kuppe C, Lynch JP. 2017. Root Cortical Senescence Improves Growth under Suboptimal Availability of N, P, and K. Plant Physiology 174, 2333 LP-2347.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Schneider HM, Wojciechowski T, Postma JA, Brown KM, L�cke A, Zeisler V, Schreiber L, Lynch JP. 2017. Root cortical senescence decreases root respiration, nutrient content and radial water and nutrient transport in barley. Plant, Cell & Environment 40, 13921408.


Progress 10/01/15 to 09/30/16

Outputs
Target Audience:Graduate students and faculty at Penn State and other universities (via invited talks); scientfic community (via publications), bean breeders and agronomists via workshops and a conference. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project included training for 13 graduate students, 3 undergraduates, and 6 visiting scholars (5 from China, one from Brazil). Professional development opportunities undertaken by students include: Christopher Strock, attended the project meeting for the USAID funded Legume Innovation Lab in Puerto Rico and a legislative information session with Dr. Lynch in Washington DC. Jenna Reeger, Ph.D. student, attended a two-week course at Purdue, the Borlaug Summer Institute in in Global Food Security, and conducted an experiment at the International Rice Research Institute in the Philippines during spring 2016. Meredith Hanlon, Ph.D. student, attended and presented her research at two conferences, the Plant Membrane Biology meeting in Annapolis MD, and the American Society of Plant Biologists (ASPB) annual meeting in Austin, TX. Stephanie Klein, Ph.D. student, also attended and presented her research at the American Society of Plant Biologists (ASPB) annual meeting in Austin, TX. How have the results been disseminated to communities of interest?Results of our work have been disseminated through the listed scientific publications and invited presentations by the PIs at professional conferences at Penn State and other universities (a total of 10 invited talks in 2016). A senior Ph.D. student, James Burridge, participated in a training and knowledge sharing workshop held in Puerto Rico for Caribbean leaders of the common bean research and seed industry communities, plus agronomy and plant breeding professionals from Mozambique. Presentations and discussions dealt with evaluation techniques, new phenotyping tools and recently generated germplasm.Mr. Burridge also presented results of research on development of new stress-tolerant bean lines at the Pan-African Grain Legume and World Cowpea Conference in Livingstone, Zambia. What do you plan to do during the next reporting period to accomplish the goals?We will continue our efforts to develop molecular markers for root architectural and anatomic traits. The Wisconsin Diversity Panel (maize) will be planted under drought and control conditions for the third season at our research site in Arizona, which will provide enough data for reliable identification of markers and candidate genes. We will continue analysis of our candidate genes for rice root architectural and anatomical traits. For rice, maize, and bean, we will conduct experiments in the greenhouse and field to test the value of specific root phenes for crop performance under drought and nutrient stress. We will explore the value of a very large number of root architectures (>1023 scenarios) under various soils constraints using SimRoot and evolutionary algorithms. We will analyze data collect during the past two years on root architectures in the field of a variety of legume species used as food-security crops.

Impacts
What was accomplished under these goals? Goal 1. To assess the value of root traits in specific stress environments via empirical studies and modeling. In previous research, we developed the concept that root systems need to be efficient in terms of carbon and nutrient cost. Efficient roots can acquire the water and nutrients the plants need without competing excessively with the shoot for resources that should support yield. Under drought or nitrogen stress, it is often useful to develop deep roots that can acquire deep water and nitrogen, which leaches down the soil profile with rain. Since plants have limited resources to devote to root development, getting deeper roots has a tradeoff: they can make fewer main root axes. Maize crown roots are the largest roots in the mature maize root system. Our field and greenhouse research showed that maize plants with fewer crown roots were able to develop longer roots, supporting the idea that there is a tradeoff between length and number of crown roots. These longer roots allowed maize plants to perform better under drought stress, since longer roots can access deep soil water. A second aspect of efficient nitrogen uptake is the kinetics of nitrogen influx in various root classes. We showed that lateral and seminal roots could take up nitrogen more easily than crown roots at low N concentrations (low Km), as well as overall greater maximum N uptake (greater Imax). Lateral roots, as the dominant portion of overall root length, are responsible for the majority of N uptake. Goal 2: Identification of the genetic basis for root traits. In order to identify molecular markers that breeders can use to select plants with desirable root traits, we need high-throughput methods for measuring root traits in the field. We have extended our development of "shovelomics", a field platform for root architecture evaluation, from maize to two legumes, Phaseolus vulgaris (common bean) and Vigna unguiculata (cowpea). Field trials were conducted at Penn State and two sites in Mozambique. The time required per root crown for excavation, washing, and evaluation of 12 (bean) or 16 (cowpea) root traits varied from 4 to 11 minutes, depending on the soil type. Throughput was increased by photographing root crowns and using the image-analysis platform DIRT, which can analyze thousands of images per hour. Comparison of seedling basal root numbers from lab-germinated plants showed a correlation of 0.92 with field-grown plants assessed at flowering. Both species demonstrated strong genetic variation for root traits. Goal 3. Determination of the agroecological impacts of trait deployment Nitrogen is the single largest cost of maize production and a major pollutant of groundwater due to leaching of nitrate applied as fertilizer to agricultural fields. If crops could place their roots to capture applied nitrate more efficiently, excess nitrate would not be leaching into groundwater. However, such crops would also have to display good agronomic performance. Modeling nitrogen acquisition with structural-functional root model SimRoot showed that the optimal root architecture for nitrate uptake depended on the initial nitrate concentration of the soil, the soil type and the precipitation pattern. Maize plants with shallow root angle acquired more nitrogen in soil types with low nitrate mobility, i.e. soils with good water retention characteristics, in soils with low nitrate availability, and in scenarios with lower precipitation. Root architectures with early development of shallow seminal roots and later development of deep nodal roots performed well in most scenarios, since the shallow seminal roots could acquire N early in the season while the deep nodal roots would acquire any N that leached deeper into the soil after precipitation events.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Fernando DR, SJ Moroni, BJ Scott, MK Conyers, JP Lynch, AT Marshall. 2016. Temperature and light drive manganese accumulation and stress in crops across three major plant families. Environmental and Experimental Botany, 132:66-79.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Vejchasarn, P, JP Lynch, KM Brown. 2016. Genetic variability in phosphorus responses of rice root phenotypes. Rice�9(1), 1-16.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: York LM, M Silberbush, JP Lynch. 2016. Spatiotemporal variation of nitrate uptake kinetics within the maize (Zea mays) root system is associated with greater nitrate uptake and additive interactions with architectural phenes. Journal of Experimental Botany 67: 3763-3775.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Dathe A, JA Postma, M Postma-Blaauw, JP Lynch. 2016. Impact of axial root angles on nitrogen acquisition in maize depends on environmental conditions. Annals of Botany 118: 401-414.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Burridge J, CN Jochua, A Bucksch, JP Lynch. 2016. Legume shovelomics: high  throughput phenotyping of common bean (Phaseolus vulgaris L.) and cowpea (Vigna unguiculata subsp, unguiculata) root architecture in the field. Field Crops Research 192:21-32.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Zhu X-G, JP Lynch, DS LeBauer, AJ Millar, M Stitt, SP Long. 2016. Plants in silico: why, why now and what?an integrative platform for plant systems biology research. Plant, Cell & Environment 39:1049-1057.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Gao, YZ, JP Lynch. 2016. Reduced crown root number improves water acquisition under water deficit stress in maize (Zea mays L.). Journal of Experimental Botany 67: 4545-4557.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Fernando DR, AT Marshall, JP Lynch. 2016. Foliar nutrient distribution patterns in sympatric maple species reflect contrasting sensitivity to excess manganese. PLOS1, PLoS ONE 11(7):e0157702.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Das, A, H Schneider, J Burridge, A Martinez-Ascanio, T Wojciechowski, CN Topp, JP Lynch, JS Weitz, A Bucksch. 2015. Digital Imaging of Root Traits (DIRT): a high-throughput computing and collaboration platform for field-based plant phenomics. Plant Methods, 11:51.
  • Type: Theses/Dissertations Status: Published Year Published: 2016 Citation: Lorts, CM. 2016. Parental effects and provisioning under drought and phosphorus stress in common bean. M.S. thesis, Intercollege Program in Plant Biology, Penn State University.


Progress 01/01/15 to 09/30/15

Outputs
Target Audience:Graduate students, undergraduate students, scientists in the US and internationally, plant breeders. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project contributed to the Ph.D. training of the following students: James Burridge (US), Tania Galindo Castaneda (Columbia), Meredith Hanlon (US), Anica Massas (Mozambique), Harini Rangarajan (India), Christopher Strock (US), Jennifer Yang (US), Jenna Reeger (US), Stephanie Klein (US), and Reham Abdallah (Egypt), and the following M.S. students: Xiyu Yang (China) and Dang Ha Nguyen (Vietnam). Visiting scientists trained in our lab in 2015 include Qun Wang (China), Baoru Sun (China), Yingzhi Gao (China), Peng Liu (China) and Pitchapa Nimwatanakul (Thailand). Postdoctoral training was provided for Gustavo Silviera (Brazil). Professional development was provided to several graduate students: Tania Galindo Castaneda, Jennifer Yang and Meredith Hanlon presented posters at the American Society of Plant Biologists in MN, Stephanie Klein attended the Maize Genetics conference in IL and a high-throughput phenotyping workshop in AZ, Tania Galindo Castaneda presented a talk at the Northeastern Corn Improvement Conference at Penn State, and Jennifer Yang presented a poster at the Rhizosphere 4 conference in the Netherlands. Five students attended the Plant Biology symposium at Penn State and one presented a poster. How have the results been disseminated to communities of interest?Results have been disseminated by publication of scientific papers, reports to sponsors, and presentations at conferences. The PIs presented 19 invited talks in 2015, 10 of which were international. Graduate students have also presented talks and posters as listed in the previous section. We maintain a website http://plantscience.psu.edu/research/labs/roots with detailed protocols for root research and lists of our projects and publications. Our work has been featured in news outlets including an article in Al Jazeera on research sponsored by the Howard G. Buffett Foundation. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? It is crucial that we develop crops that are more tolerant of drought and require less fertilizer if we are to produce adequate food for a growing population. In this research, we identify new traits that can be incorporated into crops via conventional plant breeding. Much of this research takes advantage of the fact that there is large natural genetic variation within a crop species for root traits, and that this variation has not been exploited by plant breeders because of the difficulty of measuring root traits and the lack of knowledge about which traits would be beneficial under what field conditions. We remedy this knowledge gap by modeling root systems growing under different nutrient and moisture conditions to predict what root traits would be useful, and then doing experiments to test the performance of plants with different root characteristics. Using this approach, we have identified specific strategies that root systems can employ to be more efficient in getting water and nutrients. For example, to access water present in the deeper soil layers under drought and nitrogen that leaches into deeper soil with rain, it is better to select plants with roots that branch less and elongate more, so that they have the energy to grow deeper into the soil. To make it possible for plant breeders to take advantage of this information, we have developed methods for phenotypic selection (directly measuring the trait) and are developing genetic markers for marker-assisted selection (using DNA sequence). Objective 1. To assess the value of root traits in specific stress environments via empirical studies and modeling. We investigated the effect of different lateral root branching densities for nutrient and water capture in maize. Previous work with our structural-functional plant model SimRoot predicted that long sparse lateral roots would improve nitrogen and water acquisition, since longer roots would explore larger volumes of soil including deeper soil strata. We tested these ideas empirically and found that the model predicted correctly: longer and sparser lateral roots improved maize performance under both low nitrogen stress and drought in the greenhouse and in the field. Objective 2. Identification of the genetic basis for root traits. We developed improved systems for evaluating root architecture in the field to facilitate the high-throughput phenotyping required for plant breeding impact. Root crowns are excavated, split lengthwise, and photographed for analysis using the new Root Estimator for Shovelomics Traits (REST). REST software provides semi-automated image processing to extract root architectural traits from field-grown plants quickly without losing resolution. Objective 3. Determination of the agroecological impacts of trait deployment. To investigate the impact of 100 years of selection for maize being grown at ever-higher densities and fertilizer inputs, we did a study of root traits using commercially successful open-pollinated (pre-1900) and hybrid maize lines released over the past >100 years. Evidence of greater adaptation to the competition of close spacing was revealed by shallower root angles, fewer nodal roots per whorl, greater distance to branching, increased number of smaller metaxylem vessels, and greater plasticity of aerenchyma development. Results suggested that maize has already been selected for high nitrogen acquisition efficiency due to competition, but that additional improvements could be made by focusing on specific root characteristics that can be effective in this context.

Publications

  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Burton, AL, J Johnson, J Foerster, M Hanlon, S Kaeppler, JP Lynch, and KM Brown. 2015. QTL mapping and phenotypic variation of root anatomical traits in maize (Zea mays L.). Theoretical and Applied Genetics 1:93-106.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Fernando D, JP Lynch. Mn phytotoxicity: new light on an old problem. Annals of Botany 116:313-319.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Bishopp A, Lynch JP (2015) The hidden half of crop yields. Nature Plants 1: 15117.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Zhan A, Lynch JP (2015) Reduced frequency of lateral root branching improves N capture from low-N soils in maize. Journal of Experimental Botany 66: 20552065.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Zhan A, Schneider H, Lynch JP (2015) Reduced lateral root branching density improves drought tolerance in maize. Plant Physiology 168:1603-1615.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chimungu JG, Loades KW, Lynch JP (2015) Root anatomical phenes predict root penetration ability and biomechanical properties in maize (Zea mays). Journal of Experimental Botany 66: 31513162.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Miguel MA, Postma JA, Lynch JP (2015) Phene Synergism between Root Hair Length and Basal Root Growth Angle for Phosphorus Acquisition. Plant Physiology 167: 14301439.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: York LM, Galindo-Casta�eda T, Schussler JR, Lynch JP (2015) Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress. Journal of Experimental Botany 66: 23472358.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chimungu J, Maliro M, Nalivata P, Kanyama-Phiri G, Brown K, Lynch J (2015) Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.). Field Crops Research 171: 8698.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Colombi T, Kirchgessner N, Le Mari� C, York L, Lynch J, Hund A (2015) Next generation shovelomics: set up a tent and REST. Plant and Soil 388: 120.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Fernando DR, Lynch JP (2015) Manganese phytotoxicity: new light on an old problem. Annals of Botany 116: 313319.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Lynch JP, Wojciechowski T (2015) Opportunities and challenges in the subsoil: pathways to deeper rooted crops. Journal of Experimental Botany 66: 21992210.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Nord EA, Jaramillo R, Lynch J (2015) Response to elevated CO2 in the temperate C3 grass Festuca arundinaceae across ten soil orders. Frontiers in Plant Science 6: 95.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: York LM, Lynch JP (2015) Intensive field phenotyping of maize (Zea mays L.) root crowns identifies phenes and phene integration associated with plant growth and nitrogen acquisition. Journal of Experimental Botany 66: 54935505.