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Do plants have vision, too?

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In the tropical rainforest of Chile in South America, there is a kind of gifted vine called Boquila trifoliolata. They climb trees or other plants and grow, and over time, their leaves change, "just like who they are." Even, they will imitate the leaves of other plants that are separated by a certain distance and have no contact, "if they like it, they will become it."

Figure 1. The source of https://powo.science.kew.org/ taxon / urn:lsid:ipni.org:names:107230-1 / images01 in nature as early as the 19th century, naturalists discovered and described the magical function of the leaves. In the field of botany, this ability is called "mimicry". Scientists have never been able to explain the exact mechanism of how the vines do it. Ernesto Gianoli, a plant ecologist at the University of La Serena (University of La Serena) in Chile, has studied escape vines on and off for nearly ten years, and is an important scholar in this field.

In 2010, in a field survey, Gianoli accidentally found that the leaves of sheltered vines could mimic the size, shape and color of more than 20 plants. In 2014, he published a paper in the journal Current Biology, speculating that there are two possible mechanisms for leaf mimicry:

The first is the "spread of volatile chemicals". Previous studies have shown that volatile organic compounds can induce specific responses in neighboring plants [2, 3], such as the formation of secondary metabolites, plant transcriptome changes and so on. The Gianoli team thus hypothesized that some volatile chemicals in the "prototype leaves" were transmitted through the air to the leaves of the evaded rattan, affecting the gene expression of the latter, resulting in phenotypic changes.

The second is "horizontal gene transfer between plants". That is, the genes or epigenetic factors of "prototype leaves" are transmitted to the rattan through air transmission (microorganisms), plant parasitism or natural grafting to affect its character performance. The second hypothesis is put forward because, although the sheltered vine climbs the host trunk, its leaves are imitated not only by the host leaves, but also by other plant leaves closest to them. However, Gianoli did not conduct follow-up experiments to verify his hypothesis [4].

By 2021, the Gianoli team has made new progress in the research on the mimicry mechanism of the leaves of the rattan. In November, they reported in Science report (Scientific Reports) that using gene sequencing technology, they found similar microbial groups between phantom leaves and "prototype leaves", suggesting that microbes may be involved in mimicry behavior, but further experiments are needed to verify this inference.

Just then, a private scientist (civil scientist) stepped in. He came up with an incredibly simple reason for the mimicry of the rattan:

Maybe the ivy can see what the other leaves look like.

02 Jacob White from Utah, USA, does not have any scientific research background or training, but is passionate about science and plants and likes to read popular science books and research papers. On one occasion, he read two papers describing the special photosensitive structure of two species of algae. The first paper [6] suggested that the phototaxis (phototactic behavior) of unicellular Chlamydomonas Chlamydomonas algae depended on the photoreceptors in its eye spot structure (eyespot apparatus). The second paper [7] introduced that the Synechocystis cells of cyanobacteria acted like a spherical microlens (spherical microlenses), that is, the lens, allowing the cells to "see" the light source and move toward the light source. Both articles associate algae with "eye-like" structures, which leads White to think: is it possible that other plants have similar basic vision?

At this point, Franti "ek Balu" ka, a plant physiologist at the University of Bonn (University of Bonn) and Stefano Mancuso, a plant neurobiologist at the University of Florence (University of Florence), collaborated on a short review that coincided with White's view [8]: plants may have eye-like structures that provide some form of vision.

Figure 2. A review co-authored by Balu ka and Mancuso, suggesting that plants have visual function because of their unique monocular structure. Source: 10.1016 / j.tplants.2016.07.008 after paying $40 for the full text and reading, White learned more about the "plant vision" hypothesis. It turns out that as early as 1905, botanist Gottlieb Haberlandt had assumed that the upper epidermal cells in plant leaves could function as a "simple version of the eye", similar to the ocelli of insects. In the review, the author mentions the contactless mimicry ability of anti-service vines, which may be due to the fact that the vines "see" the "appearance" of their neighbors. The article further aroused White's curiosity, and he began to search the Internet for all the research on "plant vision", especially about evasive vines.

Unfortunately, professional scientists in the academic circle do not seem to be interested in this hypothesis, and no one has carried out rigorous experiments. At present, the mainstream view of pheasant mimicry is basically the chemical transfer between plants and microbial groups proposed by Gianoli. Although the visual hypothesis is shocking, it has not attracted much attention, let alone extensive research.

Jacob White decided to do the experiment himself.

To prove experimentally that evaded vines have vision, White believes that the possibility of chemical transfer between plants should be ruled out. After thinking about it for a long time, he had an idea: since the vines can imitate what leaves they see, using artificial fake plants instead of real plants to come into contact with the vines can not only "deceive" the "eyes" of the vines, but also avoid the problem of chemical transfer.

He then bought an escape vine and let it wind around another simulated plant to observe its growth. Sure enough, the anti-service vine will also try to simulate the shape of artificial leaves in the growth process! White was so excited that he immediately took the picture and sent it to one of the authors of the review, Professor Balu Qing ka of the University of Bonn. To his surprise, Balu Balu ka replied and advised him to change his imitation and find a simulated plant that was closer to a native plant in Chile. White did so, and found that the escape vine could still simulate the shape of a new artificial leaf.

After making preliminary observations, White hopes that Professor Balu ka will take over more rigorous scientific experiments. He is afraid that he is just a layman without any scientific research qualifications and will be criticized as a "civil subject" by professionals. He bought four more escape vines and planned to find a way to get them to Professor Balu ka in Germany, but the professor unexpectedly encouraged him to continue his independent experiment and gave guidance.

Just do it. White began to design more complex experiments. But at the beginning of the experimental setup there was trouble: since it is scientific research, it is necessary to arrange the experimental group and the control group, but White home space is limited, and finally can only let the avoid rattan as the control group (compared with the original). The specific experimental design is shown in figure 3: four pots of anti-service vines are placed side by side by the window and placed under two horizontal racks. At first, the vines grow independently and do not cling to any simulated plants. When the growth exceeds the first horizontal frame, let the vines wrap around the simulated plants and continue to grow. In this way, with the first horizontal frame as the boundary, White can compare the leaves of the rattan above and below the horizontal frame.

Figure 3. Experimental design of Jacob White [9]

Figure 4. Four anti-service vines tested in Jacob White's home. Source: four anti-service vines of https://www.youtube.com/ watch?v=cfB0DwquYHg&t=3s showed miraculous imitation ability. In the first year, the vines come into contact with the artificial plant, and the leaves are obviously different from those under the horizontal frame, but the imitation effect is not very good. The next year, the vines pull out more buds, and the new leaves become more like artificial leaves, but smaller. With the passage of time, the new leaves of escape vines look more and more like artificial leaves. White recorded the whole process in the form of photos and videos and sent it all to Balu photos ka. The professor replied that he would not stop doing anything, just send out a paper! So White wrote the whole research process into an article and submitted it to the journal Plant signals and behavior (Plant Signaling and Behavior)-- the editor-in-chief happens to be Franti signals ek Balu behavior ka.

Balu creative ka sent the first draft of the article to nine peer reviews, seven of whom gave feedback. The opinions of the judges were mixed, with some immediately refuting it, while others praised it and raised questions that broke the rules. But everyone agrees that the paper needs to provide more solid data. So Balu Balu ka suggested that Felipe Yamashita, a graduate student in his lab, assist White in carrying out morphological analysis. Yamashita has not studied escape vines in the past, but his subject is mainly plant intelligence (plant intelligence), so plant vision also belongs to this area. So White sent the leaves of the sheltered vine to Yamashita for measurement and inspection.

Figure 5. Leaves (A) without mimicry and leaves (B) without mimicry. The red arrow indicates the unclosed fine leaf vein. [9] morphological analysis showed that the leaves that appeared to mimic at the top of the cross frame were indeed different from the original leaves below, and there was a significant difference between the youngest leaves near the top of the rattan and the oldest leaves at the bottom. Specifically, the veinlet of the top leaf tends to connect with other leaf veins, while one end of the leaf vein of the bottom leaf tends to be open. This is the manifestation of the difference in hormone levels: hormones are involved in the formation of leaf vein graph, and the open end of fine leaf veins decreases with the growth of vines, indicating that there are different levels of hormones in mimic leaves and without any mimicry leaves. Finally, White and Yamashita revised the paper together, which was eventually accepted by the journal and published in September 2021.

Figure 6. Paper by White and Yamashita [9] this paper, jointly published by private scientist White and botany graduate student Yamashita, has caused an unexpected sensation. Faculty Opinions (formerly F1000Prime), an important international academic paper evaluation institution in the biomedical field, selected it as the recommended paper [10], classified as "new finding" and rated as "excellent" (Exceptional, the highest rating). Experts praised it as "helpful to promote the vigorous development of plant photosensitive ability research". In addition, a popular plant-themed account on Tiktok posted a video about tropical plants [11], which quoted the paper and garnered 2.3 million views and more than 600,000 likes.

There are praises and criticisms. After carefully reading the paper, researchers in the same field questioned the content itself and the publishing process.

Ernesto Gianoli--, a master in the study of evading vines, did not participate in the peer review of the paper-- he was the first to fire. He pointed out that there was a very obvious flaw in the experimental design: the confounding factor (confounding factor) was not excluded.

Gianoli believes that light and leaf age are two important confounding factors, but the experimental design does not rule out these two variables. The leaves below the frame may be in the shade all the time, so they try to grow larger in order to get as much sunlight as possible, but when the vines climb up and enter the more brightly lit space, the leaves will grow smaller to reduce water loss, and the smaller the leaf is, the more round the shape will be, the fewer rugged contours will be, and the more fake they look. If we do not rule out the interference of light, it is impossible to determine whether the change in the shape of the blade is the result of mimicry or just a smaller size. In the same way, leaves at different growth stages naturally show different morphology. therefore, the age of leaf development may also affect the final conclusion of its mimicry mechanism.

Secondly, the data analysis method used in this paper is also accused of being used improperly. John Pannell, a plant evolution biologist at the University of Lobsang (University of Lausanne) in Switzerland, pointed out that the study measured different leaf types of the same plant, indicating that the leaves are not independent of each other, while the T-test and one-way analysis of variance (one-way ANOVA) are only suitable for situations where the data are independent and do not interfere with each other. If the statistical method is used incorrectly, the resulting p value is meaningless.

The third question is about "confirmation bias" (confirmatory bias), also known as "confirmation bias". To put it simply, scientists love their hypotheses too much and hope that their theories are correct, so they selectively use experiments, collect evidence and interpret results in the direction of "hypothesis is true" in the process of verification. White and Yamashita's paper has this tendency-- there is no in-depth discussion on the rationality of plant visual mechanism, and the confounding factors in the experiment are not excluded. When analyzing the experimental results, leaves are simply divided into "simulated leaves" and "non-simulated leaves". All this shows that the author does not hold an objective and critical attitude, but just wants to believe that the visual hypothesis is correct.

However, the above problems can not all be blamed on the author, scholars are surprised that in the review process, professional editors and peer reviews did not find …... The editor and the author did not make a clear response to these questions.

The last common doubt is the lack of a conflict of interest statement: Franti signals ek Balu behavior ka, editor of Plant signals and behavior, is also a mentor to the author of the paper, Yamashita. According to the norms of paper writing, the author should state clearly what role Balu ka plays in the publication process of the paper. Only by clarifying the conflict of interest between the author and the editor can the reader judge how such conflict of interest will affect the interpretation of the results.

Adam Marcus, editor-in-chief of the famous medical website Medscape and co-founder of Retraction Watch, agrees that the conflict of interest involved in the paper should be stated in such a situation. And Balu ka should take the initiative to avoid suspicion in the process of publishing the paper and hand it over to other chief editors. The current practice is likely to have a negative impact on journals as a whole.

In response to this query, Balu Balu ka gave only a brief response: "to eliminate all possible problems, I have asked nine peer reviewers for advice."

After more than a century of silence, the "plant ocelli" hypothesis was revived by the team of Balu ka. Balu ka himself has always believed that plants have some type of vision. Before the 2016 review was published, he led the team to conduct experiments on the roots of Arabidopsis thaliana and discovered the photosensitive mechanism based on plant-specific photoreceptors. It is proposed that the "root tip monocular (root apex ocelli)" plays a function similar to that of lens cells [12], and it is further speculated that there are information conversion regions in the root system, similar to the brain structure. The light and dark information of the plant environment is analyzed through the signal transduction pathway network based on photoreceptors, and the growth direction of the root system is guided [13,14].

Therefore, it is understandable that Balu plants ka, which believes that plant roots may have vision, will support White to carry out experiments and publish papers, because this will be another important evidence to prove the "plant vision" hypothesis. The latest collaborative paper by Balu Balu ka and Yamashita re-emphasizes the theory of "plant vision". Based on his previous research and White's research, it is proposed that plant monocular evolves from algae monocular, is part of plant complex sensory system, and guides plant cognitive behavior [15].

Gianoli commented on the "plant vision" review by Balu Balu ka in 2016. First of all, in terms of the mechanism behind the pheasant mimicry, Gianoli prefers its own explanation: the transmission of volatile chemicals and horizontal gene transfer in ecological time scales-because leaf mimicry is essentially different from plant phototaxis (such as Chlamydomonas unicellular Chlamydomonas and Cystis) and leaf orientation, it is less associated with plant vision [16]. However, Gianoli does not completely deny the hypothesis that plants can see, but so far there is no convincing evidence.

In the face of Gianoli's query, Balu Qing ka explained that leaf mimicry is to change the spatial arrangement of its own structure, and the premise of change is to have a concept of the shape or size of the imitated object, and it is necessary to "see" each other's "appearance" through a certain type of vision before it can be imitated, but chemicals cannot play a role in this regard.

The two sides have always held their own views. White and Yamashita are actively defending their findings, and Yamashita says they are already planning for the next step. They want to increase the number of escape vines, improve the control group settings, reproduce the results of White experiments, and work with the Mancuso team at the University of Florence to investigate plant electrophysiology to explore whether sudden electrical activity occurs in the vines when other plants appear near them. Gianoli, on the other hand, hopes to conduct further field investigations to see if he can explain the mechanism of plant mimicry. Whatever the answer, if researchers can finally solve the mystery, the answer could become an important new foundation for biology.

Although Gianoli took the lead in questioning "civil science research", he spoke highly of the research process of Jacob White, a private scientist: "I am so excited that people can plant sheltered vines in their own homes." In fact, both Gianoli and Balu trees ka have tried to cultivate escape vines in the laboratory, but for some reason, they do not grow well, and as a result, they cannot be further studied. "as scientists, we need such a bold approach and we need to get out of the conventional framework of thinking," Gianoli said. "but at the same time, we should not forget to regulate what is evidence and what is not." [17]

"I believe that plant science will undergo great changes." "I'm proud to be one of the new articles published every day that reveal how amazing plants are," White said. [17]

reference

[1] https://www.sciencedirect.com/science/article/pii/S0960982214002693

[2] https://www.sciencedirect.com/science/article/abs/pii/S0031942208000800

[3] https://www.sciencedirect.com/science/article/abs/pii/S0169534709003000

[4] https://www.cell.com/current-biology/fulltext/S0960-9822(14)00388-1?_returnURL=https%3A%2F%2Flinkinghub.elsevier.com%2Fretrieve%2Fpii%2FS0960982214003881%3Fshowall%3Dtrue

[5] https://www.nature.com/articles/s41598-021-02229-8

[6] https://www.pnas.org/doi/10.1073/pnas.1525538113

[7] https://elifesciences.org/articles/12620

[8] https://www.cell.com/trends/plant-science/fulltext/S1360-1385(16)30093-0

[9] https://www.tandfonline.com/doi/full/10.1080/15592324.2021.1977530

[11] https://facultyopinions.com/article/740848575

[11] https://www.tiktok.com/@tallikesplants/video/7154776470370536750

[12] https://www.frontiersin.org/articles/10.3389/fpls.2015.00775/full

[13] https://linkinghub.elsevier.com/retrieve/pii/S1674205214603300

[14] https://academic.oup.com/plcell/article/24/2/551/6097134

[15] https://www.mdpi.com/2223-7747/12/1/61

[16] https://www.cell.com/trends/plant-science/fulltext/S1360-1385(16)30171-6?_returnURL=https%3A%2F%2Flinkinghub.elsevier.com%2Fretrieve%2Fpii%2FS1360138516301716%3Fshowall%3Dtrue

[17] https://www.the-scientist.com/news-opinion/can-plants-see-in-the-wake-of-a-controversial-study-the-answer-is-still-unclear-70796

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