Learn from diversity

15 February 2023

Has it ever happened to you during a trip to a country very far from yours to walk through the countryside, recognize plants that grow spontaneously in your garden but notice so many different variations in morphology, colour, way of developing? This happens because plant populations that belong to the same species, but develop and reproduce in territories with different geographical and environmental characteristics, adapt genetically to their surroundings by changing their morphology, metabolic and physiological processes (phenotype).

Plants must adapt to the environment to survive

The genetic heritage of populations living in different geographical and environmental conditions therefore tends to adapt, to shape itself to respond to the different environmental conditions to which biological organisms are exposed. This is particularly important for plants, which are unable to move from the point where the seed has germinated, which cannot escape the heat of the sun, cold, frost, rain, drought. Their genes must change from generation to generation so that the plant can adapt as much as possible to the environmental conditions of the geographical region in which it lives: in a region where there are frequent rains it must be able to tolerate frequent flooding, in arid it will have to survive with little water, in environments where light intensity is very low, such as a dense forest, it must maximize the efficiency of the photosynthetic apparatus to continue growing and reproducing in non-optimal conditions.

The processes of adaptation and domestication are a huge experiment in the field

This adaptation process translates into the accumulation of advantageous (adaptive) mutations at the level of DNA sequences which progressively improve the plant’s ability to live and reproduce in a given environment. These DNA sequence variations occur randomly, but only those that give an adaptive advantage are fixed in the population, while those that affect important functions are lethal and therefore lost. Adaptive mutations are not randomly distributed on all genes but accumulate particularly on regulatory genes, such as transcription factors, which are able to orchestrate and direct the expression of many genes simultaneously and in a coordinated way. It is intuitive that from an evolutionary point of view, the mutation of a gene that controls many other genes is cheaper and more effective than having to accumulate sequence mutations in many genes simultaneously. This process is risky, however, because the mutation cannot drastically change the function of the regulatory gene otherwise it is lethal. The final effect is that only those mutations are accumulated that subtly change the function of the regulator, perhaps in the domains of interaction with other proteins or in the DNA binding site, or change the way in which this regulator is expressed, i.e. the moment in which it is expressed, in response to what or where, i.e. in which cell or tissue of the plant, at which moment of development.

Transcription factors as main targets in adaptation processes

In our laboratory in Rome we study the mutations of transcription factors which, from functional studies in model species, we know are at the top, at the highest hierarchical level in the gene regulation (master regulators) of important traits of the plant which influence the production and resilience to climate change of agricultural plants used for human nutrition. We try to learn from the diversity accumulated over thousands of years in natural populations or domesticated varieties, by looking for those variants (alleles) of genes encoding transcription factors that could change their function and that have been fixed in populations. The diversity of natural or domesticated populations is a huge evolutionary experiment in molecular biology and genetics. In this experiment, thousands of mutations are tested in the field for their ability to make plants more suitable for that specific environment, to be able to compete for the resources necessary for their survival and reproduction, or to improve a trait useful to man. Only those that confer an advantage are fixed, and they show us the way for the genetic improvement of cultivated species. In fact, the allelic variants found in natural populations, which can confer, for example, greater resistance to stress and adaptability to adverse climatic conditions, can be transferred (introgression) into cultivated species to make them more resilient. It thus happens that one can discover that the compact head of iceberg lettuce is the result of mutations in two transcription factors of the TALE class, studied for many years in our laboratory for their role in leaf morphology, which change the dorsal-ventral identity of the leaves and cause them to curve inward instead of outward. These two mutations, randomly selected during domestication, have made it possible to obtain a horticultural product of great value, which lasts a long time because, due to its compact head, it is not very accessible to pathogens and more capable than romaine lettuce, for example, of retaining water and maintain its characteristics of freshness and fragrance for a long time in our refrigerators. A point mutation (of a single nucleotide) in the regulatory region of a gene of the same family of plant regulators TALE, called REPLUMLESS (RPL/BLH9), is responsible for the ability or inability of the plant to disperse seeds (dehiscence) in rice and in other cereals. This character of domestication has been extremely important in agriculture because, for example, it has allowed the mechanization of the harvest of cereals, which remain enclosed in the ears instead of being dispersed into the environment. A mutation in the same nucleotide has been identified in several domesticated species of the Brassicaceae family, such as turnip (Brassica napus), which do not disperse seeds, while genetically similar wild species retain the allele that allows seed dispersal. These studies demonstrate the existence of convergence mechanisms of adaptation and domestication processes on the same set of regulatory genes important for the plant, and teach us scientists involved in genetic improvement in agriculture how important it is to learn from the diversity present in natural populations and in domesticated ones.

Until a few decades ago this was not possible because there was very little information on the DNA sequences of living organisms. Nowadays, thanks to technological advances in genetics and molecular biology, accurate and inexpensive miniaturized sequencing platforms are available, which allow us to know the DNA sequences of the genomes of many species and, within the same species, of many ecotypes (if natural populations) or cultivars / varieties (if domesticated populations). This enormous information on genetic diversity, available to all scholars in public databases, can be analyzed with the most sophisticated bioinformatics methodologies to identify advantageous allelic variants to accelerate the adaptation to climate change of cultivated species already selected for valuable characteristics for production and agri-food quality. The deep knowledge of the different classes of transcription factors, of these master regulators of the shape and architecture of the plant and of the response to environmental stress, acquired in our and other prestigious international laboratories, allow us today to “look” inside the plant genomes and recognize those variations that can have a meaning and an impact on almost every agronomic trait of the plant.

Author: Giovanna Frugis


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