Evolution of Protein Molecules

Plant diseases are responsible for major economic losses in the agricultural industry worldwide. Monitoring plant health and detecting pathogen early are essential to reduce disease spread and facilitate effective management practices. DNA-based and serological methods now provide essential tools for accurate plant disease diagnosis, in addition to the traditional visual scouting for symptoms. Although DNA-based and serological methods have revolutionized plant disease detection, they are not very reliable at asymptomatic stage, especially in case of pathogen with systemic diffusion. They need at least 1–2 days for sample harvest, processing, and analysis. Here, we describe modern methods based on nucleic acid and protein analysis. Then, we review innovative approaches currently under development. Our main findings are the following: (1) novel sensors based on the analysis of host responses, e.g., differential mobility spectrometer and lateral flow devices, deliver instantaneous results and can effectively detect early infections directly in the field; (2) biosensors based on phage display and biophotonics can also detect instantaneously infections although they can be integrated with other systems; and (3) remote sensing techniques coupled with spectroscopy-based methods allow high spatialization of results, these techniques may be very useful as a rapid preliminary identification of primary infections. We explain how these tools will help plant disease management and complement serological and DNA-based methods. While serological and PCR-based methods are the most available and effective to confirm disease diagnosis, volatile and biophotonic sensors provide instantaneous results and may be used to identify infections at asymptomatic stages. Remote sensing technologies will be extremely helpful to greatly spatialize diagnostic results. These innovative techniques represent unprecedented tools to render agriculture more sustainable and safe, avoiding expensive use of pesticides in crop protection.

/pdf/advanced-methods-of-plant-disease-detection-a-review-53f97v6zf3.pdf

Advanced methods of plant disease detection. A review

Agriculture is a specialized form of symbiosis that is known to have evolved in only four animal groups: humans, bark beetles, termites, and ants. Here, we reconstruct the major evolutionary transitions that produced the five distinct agricultural systems of the fungus-growing ants, the most well studied of the nonhuman agriculturalists. We do so with reference to the first fossil-calibrated, multiple-gene, molecular phylogeny that incorporates the full range of taxonomic diversity within the fungus-growing ant tribe Attini. Our analyses indicate that the original form of ant agriculture, the cultivation of a diverse subset of fungal species in the tribe Leucocoprineae, evolved ≈50 million years ago in the Neotropics, coincident with the early Eocene climatic optimum. During the past 30 million years, three known ant agricultural systems, each involving a phylogenetically distinct set of derived fungal cultivars, have separately arisen from the original agricultural system. One of these derived systems subsequently gave rise to the fifth known system of agriculture, in which a single fungal species is cultivated by leaf-cutter ants. Leaf-cutter ants evolved remarkably recently (≈8–12 million years ago) to become the dominant herbivores of the New World tropics. Our analyses identify relict, extant attine ant species that occupy phylogenetic positions that are transitional between the agricultural systems. Intensive study of those species holds particular promise for clarifying the sequential accretion of ecological and behavioral characters that produced each of the major ant agricultural systems.

https://www.pnas.org/content/pnas/105/14/5435.full.pdf

Major evolutionary transitions in ant agriculture

Plant pathogens can emerge in agricultural ecosystems through several mechanisms, including host-tracking, host jumps, hybridization and horizontal gene transfer. High-throughput DNA sequencing coupled with new analytical approaches make it possible to differentiate among these mechanisms and to infer the time and place where pathogens first emerged. We present several examples to illustrate the different mechanisms and timescales associated with the origins of important plant pathogens. In some cases pathogens were domesticated along with their hosts during the invention of agriculture approximately 10,000 years ago. In other cases pathogens appear to have emerged very recently and almost instantaneously following horizontal gene transfer or hybridization. The predominant unifying feature in these examples is the environmental and genetic uniformity of the agricultural ecosystem in which the pathogens emerged. We conclude that agro-ecosystems will continue to select for new pathogens unless they are re-engineered to make them less conducive to pathogen emergence.

https://tarwi.lamolina.edu.pe/~fonz/pmdas/87.pdf

The Origins of Plant Pathogens in Agro-Ecosystems

▪ Abstract Agriculture has evolved independently in three insect orders: once in ants, once in termites, and seven times in ambrosia beetles. Although these insect farmers are in some ways quite different from each other, in many more ways they are remarkably similar, suggesting convergent evolution. All propagate their cultivars as clonal monocultures within their nests and, in most cases, clonally across many farmer generations as well. Long-term clonal monoculture presents special problems for disease control, but insect farmers have evolved a combination of strategies to manage crop diseases: They (a) sequester their gardens from the environment; (b) monitor gardens intensively, controlling pathogens early in disease outbreaks; (c) occasionally access population-level reservoirs of genetically variable cultivars, even while propagating clonal monocultures across many farmer generations; and (d) manage, in addition to the primary cultivars, an array of “auxiliary” microbes providing disease suppression...

The Evolution of Agriculture in Insects

Comparisons of phylogenetic patterns between coevolving symbionts can reveal rich details about the evolutionary history of symbioses. The ancient symbiosis between fungus-growing ants, their fungal cultivars, antibiotic-producing bacteria and cultivar-infecting parasites is dominated by a pattern of parallel coevolution, where the symbionts of each functional group are members of monophyletic groups. However, there is one outstanding exception in the fungus-growing ant system, the unidentified cultivar grown only by ants in the Apterostigma pilosum group. We classify this cultivar in the coral-mushroom family Pterulaceae using phylogenetic reconstructions based on broad taxon sampling, including the first mushroom collected from the garden of an ant species in the A. pilosum group. The domestication of the pterulaceous cultivar is independent from the domestication of the gilled mushrooms cultivated by all other fungus-growing ants. Yet it has the same overall assemblage of coevolved ant-cultivar-parasite-bacterium interactions as the other ant-grown fungal cultivars. This indicates a pattern of convergent coevolution in the fungus-growing ant system, where symbionts with both similar and very different evolutionary histories converge to functionally identical interactions.

/pdf/convergent-coevolution-in-the-domestication-of-coral-3sgf5sakdp.pdf

Convergent coevolution in the domestication of coral mushrooms by fungus-growing ants

The domestication of crops and the development of agricultural societies not only brought about major changes in human interactions with the environment but also in plants9 interactions with the diseases that challenge them. We evaluated the impact of the domestication of maize from teosinte and the widespread cultivation of maize on the historical demography of Ustilago maydis , a fungal pathogen of maize. To determine the evolutionary response of the pathogen9s populations, we obtained multilocus genotypes for 1088 U. maydis diploid individuals from two teosinte subspecies in Mexico and from maize in Mexico and throughout the Americas. Results identified five major U. maydis populations: two in Mexico; two in South America; and one in the United States. The two populations in Mexico diverged from the other populations at times comparable to those for the domestication of maize at 6000–10 000 years before present. Maize domestication and agriculture enforced sweeping changes in U. maydis populations such that the standing variation in extant pathogen populations reflects evolution only since the time of the crop9s domestication.

https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2007.1636

Ustilago maydis populations tracked maize through domestication and cultivation in the Americas.

We investigated two alternative hypotheses for the origin of crop pathogen species: that human-mediated agricultural practices drove the divergence of many crop plant pathogen species or that coevolutionary processes in natural populations of the crops' ancestors drove divergence of pathogen species. We distinguished between these two hypotheses by constructing a robust multigene phylogeny and estimating the dates of divergence among four, monophyletic species of smut fungi (Ustilago maydis, U. scitaminea, Sporisorium reilianum, S. sorghi) known to specifically infect maize, sorghum, sugarcane, and their wild ancestors. Without a fossil record for smut fungi, we calibrated the pathogen species' divergence times to their plant host divergence times. Specifically, a calibration date of 10,000 years was employed to test the hypothesis that the fungal species originated at the time of domestication of their current hosts and a calibration date of 50 million years was employed to test the hypothesis that the fungal species originated on wild ancestors of their domesticated hosts. Substitution rates at five protein coding genes were calculated and rates obtained for the 10,000 year calibration date were orders of magnitude faster than those commonly reported for eukaryotes, thus rejecting the hypothesis that these smut pathogen species diverged at the time of domestication. In contrast, substitution rates obtained for the 50 million year calibration were comparable to eukaryotic substitution rates. We used the 50 million year calibration to estimate divergence times of taxa in two datasets, one comprised solely the focal species and one comprised the focal species and additional related taxa. Both datasets indicate that all taxa diverged millions of years ago, strongly supporting the hypothesis that smut species diverged before the time of domestication and modern agriculture. Thus, smut species diverged in the ecological context of natural host plant and fungal populations.

Domestication of maize, sorghum, and sugarcane did not drive the divergence of their smut pathogens

It has been postulated that the fungus Ustilago maydis followed its host maize around the world. In order to understand the biogeography of this fungus relative to its host, we used a bioinformatics approach to develop 86 tandem repeat markers useful for population studies of U. maydis. We characterized repeat motifs between two and 155 nucleotides using 36 isolates from USA, Mexico and South America. Our data suggested that (i) repeat motif length does not predict the number of alleles for that locus, and (ii) that the more polymorphic markers can resolve differences in a small geographical area.

Andrew B. Munkacsi

Papers

Convergent coevolution in the domestication of coral mushrooms by fungus-growing ants

Ustilago maydis populations tracked maize through domestication and cultivation in the Americas.

Domestication of maize, sorghum, and sugarcane did not drive the divergence of their smut pathogens

Genome-wide assessment of tandem repeat markers for biogeographical analyses of the corn smut fungus, Ustilago maydis