How did some plants become carnivorous?

For the English naturalist Charles Darwin, carnivorous plants were one of the most fascinating species due their extraordinary physiological and ecological properties. These plants live in habitats poor in nutrients –mostly on nitrogen and phosphorous- and have compensated this lack with the ability to digest animals such as insects and other arthropods.

After more than 140 years of Darwin’s publication of Insectivorous Plants, an international team identified the key genomic changes that allowed some plants to adopt a carnivorous diet, as seen in a study in which Julio Rozas, Pablo Librado and Alejandro Sánchez-Garcia, from the Faculty of Biology and the Biodiversity Research Institute of the University of Barcelona (IRBio) take part.

Adapting and surviving with a carnivorous diet in nutrient-poor soils is an evolutionary process that some evolutionary unrelated species have been going through, repeatedly and independently, from a same set of genes and proteins, according to the study published in the journal Nature Ecology & Evolution, and coordinated by Mitsuyasu Hasebe and Kenji Fukushima (National Institute for Basic Biology, Japan), Shuaicheng Li (City University of Hong Kong, China), and Victor A. Albert (University at Buffalo, United States).

Discovering the genetic mechanisms that make carnivorous diets possible

All plants are photosynthetic organisms, that is, they turn transform the inorganic matter of the environment into organic molecules (glucose). To complete the lack of nutrients of some soils, carnivorous plants can catch and absorb nutrients from a prey, thanks to an exclusively biological mechanism.

The experts have sequenced the genome of the pitcher plant (Cephalotus follicularis), an Australian species that can be identified for its insectivorous leaves –pit-fall traps that catch insects-, very different from the other leaves. The genome of this species –the second carnivorous plant with the complete genome sequenced after Utricularia gibba- is relatively large, and consists of 1,6 Gb, which is almost half of the human genome. The researchers have identified more than 36.000 genes.

According to Professor Julio Rozas, from the Department of Genetics, Microbiology and Statistics, “these plants’ ability to feed from animals in poor soils is the result of the action of natural selection, which independently favoured several genetic changes on the same set of genes. With the comparative analysis of differentially expressed genes in these two kinds of leaves, the genetic changes related to plants’ carnivorous diet have been identified”.

“According to the results, leaves that catch insects have gained new enzymatic functions: basic chitinase, which breaks down chitin (main component of insects’ exoskeleton), and purple acid phosphatase which releases phosphate groups from molecules, and it contributes to the mobilization of the prey’s phosphate”, says professor Julio Rozas, who leads the Evolutionary Genomics and Bioinformatics research group at the University of Barcelona and the platform Bioinformatics Barcelona (BIB).

Carnivorous plants: parallel evolution

Natural selection has acted on specific evolutionary routes so that plants can feed from animals. According to Dr Alejandro Sánchez-Gracia, “In addition to developing a a different strategy to catch animals, natural selection has also often acted recurrently on the same parts of particular pitcher plant genes in order to gain the ability to digest the prey, a phenomenon known as ‘parallel evolution’”.

The case of these carnivorous plants is a clear example of convergent evolution, probably due the heavy biological restrictions imposed by extreme nutrient-poor ecosystems. Moreover, the fact that this convergence was accompanied by a parallel molecular evolution in digestive enzymes makes this system an interesting example from the perspective of the study of the evolutionary process. “The examples of parallel evolution at a molecular scale are not very common. Therefore they are very interesting to understand the genetic causes of molecular adaptation and their study can help us to determine the relative role of the different evolutionary forces in biological diversification” says Sánchez-Gracia.

The evolutionary journey of plants towards a carnivorous diet

Which molecular strategies have carnivorous plants used as an adaptive evolutionary response? In their adaptation to the carnivorous diet, the generation of new genes is not always necessary: already existing genes in the plant genome have acquired new biological functions, a process known as co-option.

According to the expert Pablo Librado, “in the study, we have stated that genes originally involved in the defence against certain diseases –or the response to biotic and abiotic stress- have acquired new functions (co-option) related to the ability of feeding from animals. This is the case, for instance, of a specific set of proteins that evolved to act as digestive enzymes”.

“The results of co-option, regarding both the digestive enzymes and the amino acid changes seen in these enzymes, show that evolution has acted on a limited number of evolutionary routes in the adaptive transition to the carnivorous diet” explains Librado, who is currently working at Center for Geogenetics, from the University of Copenhagen and the Natural History Museum of Denmark.

BadiRate, a bioinformatics software created at the University of Barcelona
As part of the research, the experts of the UB and IRBio have remarkably contributed to the genomic analysis, integrating the uncertainty that exists on the species’ phylogenetic relations to infer which type of genes have preferentially duplicated or lost in the different plant species. This genomic analysis was carried out mainly with BadiRate, a bioinformatics software created by Pablo Librado and Julio Rozas (University of Barcelona) that proved to be essential to discover which kinds of genes, including digestive enzymes, recurrently accompanied the emergence of carnivorous diets in unrelated plant lineages.

Original Article

K. Fukushima, X. Fang, D. Alvarez-Ponce, H. Cai, L. Carretero-Paulet, C. Chen, T. Chang, K. M. Farr, T. Fujita, Y. Hiwatashi, Y. Hoshi, T. Imai, M. Kasahara, P. Librado, L. Mao, H. Mori, T. Nishiyama, M. Nozawa, G. Pálfalvi, S. T. Pollard, J. Rozas, A. Sánchez-Gracia, D. Sankoff, T. F. Shibata, S. Shigenobu, N. Sumikawa, T. Uzawa, M. Xie, C. Zheng, D. D. Pollock, V. A. Albert, S. Li, M. Hasebe. «The pitcher plant Cephalotus genome reveals genetic changes associated with carnivory». Nature Ecology & Evolution, 2017

Image: According to this study, natural selection has taken similar evolutionary routes so that plants can feed from other animals to complete their diets.