Old Growth. Tionesta, PA. Photo by Nicholas T, Flickr
(Click on the following link to listen to an audio version of this blog …. Can Plants See?
The ability of plants to sense their environments and communicate both with each other and also with the animals around them are topics of great interest in both popular and scientific literature. Peter Wohlleben, in his book Hidden Life of Trees writes about trees communicating with each other via the “wood wide web” of mycorrhizal fungal connections. The interconnected trees of a forest, according to Wohlleben, form “friendships” and care for each other. Wohlleben also talks about parental trees that “love” their offspring, and about trees that exhibit “pity,” or who were “bullies,” or “cold and unfeeling.” (see Signs of Fall 10, November 21, 2019). Monica Galiano in her book Thus Spoke the Plant and in a number of published, scientific journal articles has explored the consciousness and intelligence of plants and their abilities to both perceive environmental stimuli and communicate (see Signs of Fall 11, November 28, 2019).
Very recently, a paper published in Cell (March 30, 2023) and then covered by many major news outlets, involved a team of researchers at Tel Aviv University in Israel who noted that plants make ultrasonic sounds when they were stressed. Lack of water and the trauma of having their stems cuts (simulating the physical damage caused by herbivory) generated these distress calls in both tobacco (Nicotiana tabacum) and tomato (Solanum lycopersicum) plants.
Along with these chemical, tactile and auditory sensory systems, it has been proposed that plants are also capable of vision. Previously, eyespots were have been described in the green algae (Chlamydomonas reinhardtii) which help control its phototactic behavior. Also, photoreceptors have been described in unicellular cyanobacteria that enable them to move toward light. Further, back in 1905, the botanist Gottlieb Haberlandt hypothesized the upper epidermal cells of plant leaves may function as primitive, visual receptors. But, until recently, no specific research on green plants has demonstrated that plants are able to see.
Boquila trifoliolata. Photo by Inao. Wikimedia Commons
A paper published in Plant Signaling and Behavior (September 21, 2021) explored the remarkable ability of a vine that grows in the temperate forests of central and southern Chile and Argentina to change the shape of its leaves into mimics of the leaves of the host plant on which it is growing. This vine, Boquila trifoliolata, benefits from this mimicry because of a reduced likelihood of herbivory when it is able to “hide” in the foliage of its host. To date, B. trifoliolata has been shown to accomplish its leaf mimicry on more that twenty host plants, and it has been determined that this mimicry can occur even without direct plant-to-plant contact. It has also been shown that as a single vine grows up and around a sequence of supporting host plants, the vine is able to form leaf mimics that match the host leaves in each section of its growth.
How this mimicry is accomplished is not known. Previous hypotheses have suggested that volatile chemicals or possibly even shed nucleic acids may be originating from the host plant which then alter the growth patterns of the B. trifoliolata leaves. There is also some suggestion that bacteria in the host plants’ microbiome may be transferred to the B. trifoliolata and that they might be the source of the leaf-shaping chemicals. The authors of the Plant Signaling and Behavior article, Jacob White and Felipe Yamashita, however, believe that B. trifoliolata is able to accomplish this leaf mimicry because it can see the shapes of the host plants leaves.
Jacob White is a plant enthusiast and self-described “citizen scientist” living in Utah who became interested in the phenomenon of B. trifoliolata’s leaf mimicry. White grew a B. trifoliolata in his home (a remarkable accomplishment considering how difficult it is to grow this particular plant!). He then used an artificial plant as the vine’s host plant. An artificial plant could not emit nucleic acids or other volatile chemicals nor would it have a bacteria-rich microbiome that it could share with the growing vine. As the vine grew and matured, its leaves took on the shape of those of the artificial plant.
White sent photographs of his vine and the artificial plant that it mimicked to Frandisck Baluska of the University of Bonn, Germany. Baluska had co-authored a 2016 journal article in which he suggested that plants had eye-like organs and were capable of vision. Baluska responded positively to White’s photographs and suggested that he repeat his experiment with an artificial plant that more closely resembled some of the natural host plants that B. trifoliolata would encounter in its native habitat. White agreed and the results of this second trial once again demonstrated a significant degree of mimicry by B. trifoliolata.
B. trifoliolata. Photo by S. Zona. Wikimedia Commons.
With these preliminary results, White wanted to set up a more elaborate experiment but was limited both by space (he was working in his home and could only dedicate a small room to the experiment), and a suitable growth system (his experimental room only had a single, sun-lit window where he could reasonably grow the vines). He was also limited by the number of B. trifoliolata plants that were available to him (as I previously mentioned, these plants are notoriously difficult to grow!). He only had four plants and, so, could not run multiple replications of his treatments or even set up reasonable controls.
He constructed a series of shelves by the window and planned to have his B. trifoliolata grow from a lower shelf (where it was not in contact with any host plant (this would be his control)) to a higher shelf (where he would expose the vine to an artificial plant). He would then compare the leaves of the lower section of the vine to the leaves of the higher section of the vine in order to determine the degree of induced mimicry. After two years of growth, the B. trifoliolata leaves from the upper shelf were different in shape from the leaves growing in the lower shelf, and the upper shelf leaves resembled the leaves of the experimental, artificial plant.
Baluska encouraged White to write up his results and submit them to the journal Plant Signaling and Behavior where he, Baluska, was an editor-in-chief. White wrote the paper and submitted it to the journal. Baluska sent the paper out to nine reviewers. The responses of the reviewers ranged from praise for the originality of the experiment to outright rejection. All reviewers, though agreed that the paper needed more precise data concerning the different shapes of the leaves.
Baluska then matched White up with one of his graduate students, Felipe Yamashita, who was doing research on plant intelligence, in order to generate more precise data from White’s B. trifoliolata experiment. Yamashita’s analysis confirmed White’s observations on B. trifoliolata leaf mimicry: the leaf shapes in the vine segments of the upper and lower shelves were different and the upper shelf leaves resembled the leaf shapes of the artificial host plant. Baluska accepted the re-written paper for publication. He did not, however, indicate on the paper his participation in developing or directing White’s research. He also did not indicate that Yamashita was one of his graduate students. Both of these omissions might be interpreted as attempts to hide a significant conflict of interest on the part of Baluska.
The published paper also was subject to severe criticisms. The lack of proper controls, and the likelihood that the shelves on which the plants were growing generated different degrees of shading and, possibly, temperature. Also the statistical analysis used required that the variables being measured and compared were independent of each other, and independence is difficult to assume when leaves from different sections of the same plant are being compared. Also, the small sample size made statistical analysis difficult, and the small number of photographs published illustrating the leaf types were all considered to be significant flaws in this paper.
Range of leaf mimics in B. trifoliolata. Photo by E. Gianoli and F. Carrasco-Urra. Current Biology
As Ernesto Gianoli, the Chilean botanist who first described the remarkable mimicry in B. trifoliolata and who, very surprisingly, was not asked by Baluska to review this paper, put it “(this is) a textbook case of confirmatory bias. The scientists fell in love with their hypothesis. . . Once you are in love with your hypothesis, you force the systems to validate your view.” White and Yamashita have found something, but their experiment was so flawed that the nature of this something is not clear.
New experiments on B. trifoliolata are planned by Yamashita in Baluska’s University of Bonn laboratory, but the botanical garden of the university is having difficulties growing sufficient B. trifoliolata for these studies. Gianoli, who has also been unable to grow viable B. trifoliolata in his laboratory, hopes to continue to do field studies on the vine. Both research groups feel that there is some new and fundamental feature about this plant that controls its ability to mimic so many different types of leaves, and that uncovering this mimicry-mechanism may lead to a deeper understanding of the complexity and physiological elegance of plants.