RESEARCH
Our lab combines evolutionary ecology, quantitative genetics, and genomics to study symbiosis and environmental adaptation. Understanding how symbiotic partners co-evolve and adapt to different environments is ecologically and agriculturally important. For example, this will help us explain how cooperation is maintained in the symbiosis between plants and rhizobium bacteria, which is responsible for half of all current biologically fixed terrestrial nitrogen. In this symbiosis, host plants trade photosynthetically derived carbon for nitrogen fixed by endosymbiotic rhizobium bacteria housed in root nodules.
I. EVOLUTION DURING DOMESTICATION
How does symbiosis change during domestication?
- We are taking a comparative approach to contrast crops’ ability to benefit from microbial symbiosis to that of their wild relatives by integrating phylogenetics, microbial genetics, quantitative genetics, and genomics. Beneficial microbes that colonize plants play key roles in plant health, yet little is known about how a plants’ ability to benefit from cooperative microbes changes during domestication. Plant-microbe cooperation is unstable. Plants have repeatedly abandoned cooperation with microbes over evolutionary time, and evidence from my lab shows that crops can evolve to interact differently with beneficial microbes than do their wild relatives. This reveals a gap in scientific understanding of the evolution of cooperation: what evolutionary processes result in changes to plant symbiosis traits along the path to development of a cultivated crop?
- To investigate declines we observe in plant benefits from microbial symbiosis during crop domestication and improvement, we are using US National Plant Germplasm System collections, recombinant inbred line populations, and genomic resources for legume crops ranging from soybeans to peas as model systems. The agricultural utility of legumes lies in their unique symbiosis with rhizobium bacteria, which convert atmospheric nitrogen into useable forms, essentially fertilizing the plant. At least forty-one legume species have been domesticated. Understanding how and why the rhizobial symbiosis evolves during domestication will provide a critical road map for ways in which we could improve crop benefits from microbes in order to increase US and global food security
Related papers:
Porter SS et al, (in revision) Host-imposed control mechanisms in the legume-rhizobia symbiosis, Nature Microbiology
Millar N et al (2023) Impacts of domestication on the legume-rhizobium mutualism, Plant and Soil, https://doi.org/10.1007/s11104-023-06128-x
Montoya A et al (2023) Hosts winnow symbionts with multiple layers of absolute and conditional discrimination mechanisms, Proceedings of the Royal Society B, https://doi.org/10.1098/rspb.2022.2153
Helliwell E et al (2022) Transgenic soybeans secreting phosphatidylinositol-3-phosphate-binding proteins show enhanced resistance against the oomycete pathogen Phytophthora sojae, Frontiers in Microbiology, Vol. 13, https://doi.org/10.3389/fmicb.2022.923281
Klein M et al (2021) Evolution of manipulative microbial behaviors in the rhizosphere, Evolutionary Applications, 00:1-16, DOI: 10.1111/eva.13333 KleinEtAl2021
Porter SS & Sachs JL (2020) Agriculture and the disruption of plant-microbial symbiosis, Trends in Ecology and Evolution Porter&Sachs2020, see press
II. EVOLUTION OF SYMBIOTIC MICROBIAL DIVERSITY
How do wild microbes adapt to the environment?
- To understand the origin and diversification of microbial life, we use a combination of experiments, natural history, genetics, and population genomics. Bacteria thrive in extreme environments that require them to tolerate stresses ranging from toxic heavy metals in the environment to assault from host immune systems in symbiosis with host organisms. The genetic basis of bacterial adaptation to such diverse environments is largely undescribed in natural systems, yet this information is critical for understanding the generation and functional significance of bacterial diversity.
- Diversity persists if the genes or traits that underlie adaptation to one environment diminish fitness in another environment. This fitness tradeoff can promote niche specialization and prevent competitive exclusion. However, bacteria have modular, fluid genomes—adaptive genes are rapidly horizontally transmitted between strains. This can allow adaptive variants to assort across environmental gradients without the constraints that limit both allelic substitution and exploration of the adaptive landscape in macro-organisms. Whether trade-offs are critical to the generation and maintenance of microbial diversity remains a frontier in Evolutionary Biology.
- We aim to link the genomic, physiological, and ecological bases of local adaptation to heavy metal enriched serpentine soils in several clades of wild symbiotic Mesorhizobium bacteria. We have identified candidate genes for heavy metal adaptation in wild Mesorhizobium bacteria are leveraging association mapping and molecular genetic approaches to dissect the genetic basis of heavy metal adaptation. These Mesorhizobium symbiotically fixing nitrogen for native legume species and our system serves as an emerging bacterial model of adaptation that will lead to innovative strategies to incorporate metal-adapted soil microbiota in bioremediation of heavy metal contaminated soils.
Related Papers:
Kehlet-Delgado H et al (in press) The evolutionary genomics of adaptation to stress in wild rhizobium bacteria, Proceedings of the National Academy of Sciences
Porter SS (2021) Dispatch: Symbiont switching and environmental adaptation, Current Biology, 31(17):R1049-R1050, https://doi.org/10.1016/j.cub.2021.07.079 Porter2021
Martinez ML et al (2021) Specialization in multiple niche axes supports the oscillation theory of speciation in native legumes, Evolution, 75(5):1070-1086, https://doi.org/10.1111/evo.14222 MartinezEtAl2021
Porter SS et al (2020) Beneficial microbes ameliorate abiotic and biotic sources of stress on plants, Functional Ecology, doi.org/10.1111/1365-2435.13499 PorterEtAl2019, see press
Porter SS et al (2018) Dynamic genomic architecture of cooperation in a wild population of Mesorhizobium, ISME J PorterEtAl2018
Porter SS et al (2017) Association mapping reveals novel serpentine adaptation gene clusters in a population of symbiotic Mesorhizobium, ISME, doi: 10.1038/ismej.2016.88 PorterEtAl2016
Jones EI et al (2015) Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism. Ecology Letters, 18(11):1270-1284. JonesEtAl2015, see press
Friesen ML et al (2014) The Ecological and Genomic Basis of Salinity Adaptation in Tunisian Medicago truncatula, BMC Genomics, 15(1):1160. FriesenEtAl2014
Porter SS & Simms EL (2014) Selection for cheating across disparate environments in the legume-rhizobium mutualism, Ecology Letters 17: 1121-1129. PorterSimms2014
Ehinger M et al (2014) Specialization-generalization trade-off in a Bradyrhizobium symbiosis with wild legume hosts, BMC Ecology 14:8. EhingerEtAl2014
Porter SS (2013) Adaptive divergence in seed color camouflage in contrasting soil environments, New Phytologist, 197:1311-1320. Porter2013
Porter SS & Rice KJ (2013) Trade-offs, spatial heterogeneity, and the maintenance of microbial diversity, Evolution, 67(2): 599-608. PorterRice2013
Friesen ML et al (2011) Microbially Mediated Plant Functional Traits. Annual Review of Ecology, Evolution, and Systematics vol. 42:23-46. FriesenEtAl2011
III. MUTUALISM EVOLUTION UNDER GLOBAL CHANGE
How do microbial symbionts affect biological invasions?
- Invasive species wreak havoc on ecosystems by displacing natives and by altering abiotic conditions. While much is known about the substantial harm invasive plants and animals inflict, we know little about the impacts of the invisible communities of microbial mutualists that co-invade with their hosts or how host-symbiont mutualisms are re-shaped at genomic and ecological levels during biological invasions.
- The legume-rhizobium symbiosis is an ecologically important model mutualism amenable to addressing these fundamental questions. Medicago polymorpha, a noxious legume weed and a relative of alfalfa, has co-invaded North America from Europe with its rhizobial partner, Ensifer medicae.
- These co-invading mutualists have experienced dramatically different population genomic consequences of invasion. While the plant shows substantial reductions in genomic diversity in the invaded range relative to populations in the native range, its symbiont has not experienced a similar bottleneck in genomic diversity during invasion. We find that robust cooperation between the partners is unaltered by the process of invasion, yet the partners show reduced genetic variance in mutualistic traits in the invaded range. Therefore, the mutualism functions similarly in the invaded and native range, but has a lower capacity for cooperation to evolve in the invaded range. We also find that low symbiont abundance in the soil is a key ecological attribute slowing the spread of this noxious weed and that the success of this weed not only depends upon symbiont nitrogen fixation, but also benefits from symbiont mediated protection from soil pathogens.
Related Papers:
Wendlandt C et al (2022) Negotiating mutualism: a locus for exploitation by rhizobia has a broad effect size distribution and context-dependent effects on legume hosts, J Evolutionary Biology, 00:1-11, https://doi.org/10.1111/jeb.14011
Wendlandt C et al (2021) Decreased coevolutionary potential and increased symbiont fecundity during the biological invasion of a legume-rhizobium mutualism, Evolution, http://dx.doi.org/10.1111/evo.14164 WendlandtEtAl2021
Lopez Z et al (2020) Patchy symbiont distribution constrains the fitness of an exotic plant across an invaded landscape, Biological Invasions, doi.org/10.1007/s10530-020-02404-4 LopezEtAl2020
Jack CN et al (2019) Rhizobia Protect Their Legume Hosts Against Soil-Borne Microbial Antagonists in a Host-Genotype-Dependent Manner, Rhizosphere, 9:47-555, DOI: 10.1016/j.rhisph.2018.11.005 JackEtAl2019
Jack CN et al (2019) A high-throughput method of analyzing multiple plant defensive compounds in minimized sample mass, Applications in Plant Sciences, 7(1): e1210, DOI: 10.1002/aps3.1210 JackEtAl2019
Krieg CP et al (2019) Nitrogen fixation: Fixing the gap between concept- and evidence-based learning with legume biology, American Biology Teacher, 81(4):250-255, DOI: 10.1525/abt.2019.81.4.250 KriegEtAl2019
Helliwell E et al (2019) Rapid establishment of a flowering cline in Medicago polymorpha after invasion of North America, Molecular Ecology, DOI: 10.1111/mec.148 HelliwellEtAl2018
Porter SS et al (2018) Co-invading symbiotic mutualists of Medicago polymorpha retain high ancestral diversity and contain diverse accessory genomes, FEMS Microbial Ecology PorterEtAl2018
La Pierre KJ et al (2017) Invasive legumes can associate with many mutualists of native legumes, but usually do not, Ecology and Evolution, DOI: 10.1002/ece3.3310 LaPierreEtAl2017
Amsellem L et al (2017) Importance of microorganisms to macroorganisms invasions — Is the essential invisible to the eye? Advances in Ecological Research (Special Issue on Networks of Invasion) AmsellemEtAl2016
Porter SS et al (2011) Mutualism and adaptive divergence: Co-invasion of a heterogeneous grassland by an exotic legume-rhizobium symbiosis, PLoS One: e27935. PorterEtAl2011