Mutations in genes that are essential for defence against predator attack are usually deleterious and would be expected to be quickly eliminated from a population, however, occasionally, the same mutation can convey an advantage which it is able to assert in conditions where predator populations are low, and this is especially true if wide genetic diversity within the population makes it more likely that the mutation can operate synergistically with other genes.
This can lead to a dynamic situation in which, in periods of low predation, the mutation can increase, or at least remain at a stable level in the population, and, in periods of high predation, it can be reduced. This dynamic can result in deleterious genes being retained in a population for much longer than would be expected if they were wholly deleterious.
An example of this was found recently by researchers from the Max Planck Institute for Chemical Ecology, Jena, Germany, in a wild member of the tobacco family, Nicotiana attenuata. Their finding is published in Proceedings of the National Academy of Science (PNAS)
The research and its significance are explained in a press release:
In a recent study in PNAS, a team of researchers at the Max Planck Institute for Chemical Ecology in Jena, Germany, shows that a single mutation that has immediate effects on plant fitness is maintained over the long term in natural plant populations, despite theories predict the contrary. The researchers located and identified the gene that regulates the amount of an active defense hormone. Mutants in this gene are susceptible to herbivore attack. However, they compensate for impaired defenses through robust genetic networks. When fewer herbivores attack, they even grow faster and produce more offspring (PNAS, August 2023, doi: 10.1073/pnas.2308500120).Technical detail is explained in the teams abstract to their paper in PNAS:
Plants are not exposed to herbivores without defenses. When an insect feeds on a leaf, thereby wounding it and releasing oral secretions, a signaling cascade is elicited in the plant, usually starting with a rapid increase in the amount of the plant hormone jasmonic acid and its active isoleucine conjugate. Jasmonic acid regulates various reactions in plants, including defenses against herbivores and responses to environmental stress.
Mutants with disadvantageous properties do not necessarily disappear
An important thesis of evolutionary theory is natural selection and the conclusion that mutants with disadvantageous properties disappear again. However, researchers at the Max Planck Institute for Chemical Ecology in Jena have made observations on the wild tobacco species Nicotiana attenuata, also known as coyote tobacco, that contradict this prediction.Coyote tobacco Nicotiana attenuata is a plant species native to the Great Basin Desert of the western United States. Natural populations of this wild tobacco contain plants with significant mutations in their defenses against herbivores. These mutants are more susceptible to insect attack but grow faster. They can also compensate for the reduced defenses due to robust genetic networks.© Ian T. Baldwin, Max Planck Institute for Chemical Ecology
Twenty years ago, the scientists conducted field trials with tobacco plants muted in their defense signals in their natural environment, the Great Basin desert in the U.S. state of Utah. These genetically modified plants attracted leaf hoppers of the genus Empoasca, which were not found on wild type plants whose defenses had not been impaired. At the same time, the researchers observed that feeding damage by leaf hoppers could also be observed on some individuals in natural populations. They showed that natural defense mechanisms in these individual plants were compromised. However, the research team also found that other defense-impaired mutants exposed to only few herbivores in the field grew significantly faster than those with intact defense signals did. However, in years of high herbivore pressure, the mutants were so severely attacked that they did not survive and were unable to reproduce.
To test this hypothesis, Ian Baldwin's team developed what is called a MAGIC population, which captures a large portion of the genetic diversity of the entire Nicotiana attenuata species in a breeding population with a homogenized genetic background. Creating this population required screening hundreds of natural plant accessions from seed collections at different locations in the Great Basin Desert over three decades to eventually select 26 very different parental lines that were crossed with each other in a very structured way for a decade. The result of these crosses is the MAGIC (multi-parent advanced generation inter-cross) population. In addition, the researchers created a high-quality coherent reference genome.These findings led us to think that natural populations of Nicotiana attenuata might contain natural mutants in the defense signaling pathway and that these mutants were maintained in natural populations by trade-offs between growth- and defense-related selection pressures.
Ian T. Baldwin, senior author. Department of Molecular Ecology
Max Planck Institute for Chemical Ecology, Jena, Germany
Priority of growth and reproduction over defense becomes an advantage in years with little herbivore pressure
With this data set, the scientists were able to accurately map the genetic basis of the higher susceptibility to herbivores and the variation in the levels of the jasmonic acid conjugate and locate the causative mutation in the genome.In Nicotiana attenuata plants, variation in the JAR gene affects how much of the jasmonic acid conjugate is accumulated. A mutation in this gene results in lower levels than in normal plants. The mutants prioritize growth and reproduction over defense, making them more susceptible to insect attack but potentially better at growing fast and producing more offspring.
Rishav Ray, first author
Department of Molecular Ecology
Max Planck Institute for Chemical Ecology, Jena, Germany
In addition, the researchers demonstrated that the mutation in this single gene responsible for plant defense signaling is maintained in a population for at least 10 years, and a robust genetic network can buffer the deficit in defense, allowing the mutants to survive in nature.
Genetic mutations occur constantly and are, by and large, randomly distributed throughout genomes. Most often, these mutations are detrimental, but occasionally they are responsible for helpful traits in mutants that facilitate survival in certain environments. In this case, as suggested in the present study, the main mutation may be part of a robust genetic network and lead to the accumulation of other mutations with large effects. This increases genetic diversity in natural populations, which is important for their long-term survival and success in the rapidly changing environments of our planet.With the planet’s rapidly changing climate, it is essential to understand and identify how natural processes have maintained genetic diversity so that we can find better ways of protecting and preserving the remaining biodiversity on our planet.
Ian T. Baldwin.
The extensive population sampling carried out 30 years ago in the Great Basin desert by the scientist, who has been investigating the survival strategies of this wild tobacco species for decades, was crucial to the success of the study. The study shows that even after many years the collection and storage of such samples can still prove valuable, and emphasizes the importance of funding such long-term research projects.
SignificanceCreationists will tell you that all mutations are deleterious because their dogma says so; science shows us that even normally deleterious mutations can be beneficial in the right environment.
Single-gene mutations with large fitness effects are found in natural populations, contrary to theoretical expectations: understanding how these fitness effects are buffered would complement the functional explanations of balancing selection for their maintenance. Jasmonate (JA) signaling mediates many environmental responses in higher plants; the formation of its central ligand, jasmonoyl-L-isoleucine (JA-Ile), was thought to be invariable. In natural populations of native tobacco plants, we uncover a major mutation in forming JA-Ile; demonstrate its molecular basis, biochemical function, fitness consequences, and find it maintained in several populations over a decade of sampling. When highly connected hub genes were silenced from a coexpression network, JA-mediated defense responses varied with distance from the mutation, consistent with its embedding in a gene regulatory network.
Abstract
When insect herbivores attack plants, elicitors from oral secretions and regurgitants (OS) enter wounds during feeding, eliciting defense responses. These generally require plant jasmonate (JA) signaling, specifically, a jasmonoyl-L-isoleucine (JA-Ile) burst, for their activation and are well studied in the native tobacco Nicotiana attenuata. We used intraspecific diversity captured in a 26-parent MAGIC population planted in nature and an updated genome assembly to impute natural variation in the OS-elicited JA-Ile burst linked to a mutation in the JA-Ile biosynthetic gene NaJAR4. Experiments revealed that NaJAR4 variants were associated with higher fitness in the absence of herbivores but compromised foliar defenses, with two NaJAR homologues (4 and 6) complementing each other spatially and temporally. From decade-long seed collections of natural populations, we uncovered enzymatically inactive variants occurring at variable frequencies, consistent with a balancing selection regime maintaining variants. Integrative analyses of OS-induced transcriptomes and metabolomes of natural accessions revealed that NaJAR4 is embedded in a nonlinear complex gene coexpression network orchestrating responses to OS, which we tested by silencing four hub genes in two connected coexpressed networks and examining their OS-elicited metabolic responses. Lines silenced in two hub genes (NaGLR and NaFB67) co-occurring in the NaJAR4/6 module showed responses proportional to JA-Ile accumulations; two from an adjacent module (NaERF and NaFB61) had constitutively expressed defenses with high resistance. We infer that mutations with large fitness consequences can persist in natural populations due to compensatory responses from gene networks, which allow for diversification in conserved signaling pathways and are generally consistent with predictions of an omnigene model.
Ray, Rishav; Halitschke, Rayko; Gase, Klaus; Leddy, Sabrina M.; Schuman, Meredith C.; Rodde, Nathalie; Baldwin, Ian T.
A persistent major mutation in canonical jasmonate signaling is embedded in an herbivory-elicited gene network
Proceedings of the National Academy of Sciences; 120(35) e2308500120. DOI:10.1073/pnas.2308500120
Copyright: © 2023 The authors.
Published by PNAS Open access.
Reprinted under a Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND 4.0).
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