A hypothesis on the capacity of plant odorant-binding proteins to bind volatile isoprenoids based on in silico evidences

  1. Deborah Giordano
  2. Angelo Facchiano
  3. Sabato D'Auria
  4. Francesco Loreto

  • Curated by eLife

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    Evaluation Summary:

    The chemical sensing mechanisms of plants, which are largely unknown, are a topic of broad interest. The authors hypothesise that plant chemical receptors may be transporter proteins or odorant binding proteins analogous to those found in animals. The authors have identified a list of plant proteins with possible odorant binding activity and they predict binding constants for relevant odorants. The calculated binding constants are generally very weak in comparison to known animal odorant binding proteins (i.e., would require much higher concentrations of odor for detection). The in silico investigation, while inspiring, leaves many open questions, for example whether or not there is evidence for functional analogy between plant and animal odorant binding proteins.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript.The reviewers remained anonymous to the authors.)

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Abstract

Volatile organic compounds (VOCs) from ‘emitting’ plants inform the ‘receiving’ (listening) plants of impending stresses or simply of their presence. However, the receptors that allow receivers to detect the volatile cue are elusive. Most likely, plants (as animals) have odorant-binding proteins (OBPs), and in fact, a few OBPs are known to bind ‘stress-induced’ plant VOCs. We investigated whether these and other putative OBPs may bind volatile constitutive and stress-induced isoprenoids, the most emitted plant VOCs, with well-established roles in plant communication and defense. Molecular docking simulation experiments suggest that structural features of a few plant proteins screened in databases could allow VOC binding. In particular, our results show that monoterpenes may bind the same plant proteins that were described to bind other stress-induced VOCs, while the constitutive hemiterpene isoprene is unlikely to bind any investigated putative OBP and may not have an info-chemical role. We conclude that, as for animal, there may be plant OBPs that bind multiple VOCs. Plant OBPs may play an important role in allowing plants to eavesdrop messages by neighboring plants, triggering defensive responses and communication with other organisms.

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  1. eLife

    Evaluation Summary:

    The chemical sensing mechanisms of plants, which are largely unknown, are a topic of broad interest. The authors hypothesise that plant chemical receptors may be transporter proteins or odorant binding proteins analogous to those found in animals. The authors have identified a list of plant proteins with possible odorant binding activity and they predict binding constants for relevant odorants. The calculated binding constants are generally very weak in comparison to known animal odorant binding proteins (i.e., would require much higher concentrations of odor for detection). The in silico investigation, while inspiring, leaves many open questions, for example whether or not there is evidence for functional analogy between plant and animal odorant binding proteins.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript.The reviewers remained anonymous to the authors.)

  2. eLife

    Reviewer #3 (Public Review):

    It is known that stress-induced plant volatiles can be perceived by neighboring plants, but the underlying mechanism is largely unknown. The authors of this manuscript attempted to identify receptors that interact with isoprenoids, the most abundant plant stress-induced volatile organic compounds (VOCs). They established a framework that allowed them to screen for plant odorant-binding proteins (OBPs) through all available databases. Comparing plant protein sequences with a large group of animal OBP sequences and expanding the investigation to previously known OBPs turned out to be fruitful. Molecular simulation is a powerful screening technique to study the interaction of the potential plant OBPs with selected isoprenoids. The finding that plant OBPs may bind different VOCs in the same binding site is interesting.

    The in silico selection of the plant OBP candidates and ligand docking experiments provide a useful tool to understand signals that underpin plant-plant interactions as well as how plants respond to those cues. However, the conclusions made by the authors may be too premature:

    Isoprenoids are both constitutive and stress-induced. The authors did not address, through such a docking study, how plants distinguish VOCs associated with impending stresses, particularly when the OBPs could generally interact with multiple VOCs. One may also wonder how many other types of VOCs exist that are stress-responsive, and what their receptors are.

    The BLAST of 432 OBPs did not find the JA receptor, suggesting that the JA receptor sequence is not closely related to that of the OBPs that insects use to recognize plant volatiles in order to locate suitable host plants. Therefore, identification of OBPs based on sequence similarity may miss those plant proteins that possess OBP structure and function but differ in primary sequences with existing OBPs.

    Docking studies can serve as a lead for potential OBP-VOC interaction, but in silico data alone is insufficient to conclude the role of the putative OBPs. Functional evidence is necessary to demonstrate their interaction with VOCs because such interaction indeed affects plant response.

  3. eLife

    Reviewer #2 (Public Review):

    The Authors started from the consideration that volatiles emitted by plants may serve as communication media to other plants. Hence, the 'receiver' plant needs a way to bind these molecules and initiate the transduction cascade, that is a dedicated protein that is able to bind volatiles because it has a binding groove able to accomodate the ligand. The Authors searched the available databases for putative proteins that can serve this goal, by similarity to already known proteins from plants and animals. Then, by molecular docking known plant volatiles, the Authors demonstrate that the identified proteins have the predicted structural features that allow ligand binding.

    The main strength of the paper resides in the idea and in the wide search for similarities among proteins pertaining to different kingdoms. The main weakness of this work resides in the fact that it is entirely in silico, without providing any actual data from real proteins. However, it is well known that in silico simulations may be only suggestive of the actual behavior of a protein.
    The Authors reached their goal of identifying various proteins with putative binding abilities, however the lack of any experimental data should be made clear since the beginning of the manuscript, in the title and abstract. With this caveat, the information provided in this paper may be a useful starting point for experimentally testing of the hypotheses.

  4. eLife

    Reviewer #1 (Public Review):

    The chemical sensing mechanisms of plants are largely unknown. The authors hypothesise that plant chemical receptors may be transporter proteins or odorant binding proteins. The authors carried out an "in silico" analysis to investigate whether there are analogous proteins in plants to odorant binding proteins found in animals and insects. A search through protein databases found 5 possible sequences or partial sequences and these were used for further screening using BLAST software for screening comparison. The search for OBPs in plants based on literature evidence and sequence similarities to known OBPs from animal organisms or database annotations , produced a list of plant proteins, or protein families, with potential OBP activity. Molecular docking simulation experiments, to identify candidate plant OBPs were carried out identifying the ligand binding sites and calculated binding energies together with binding constants. This data mining activity has produced some interesting data but also raises several questions. The majority of binding constants tabulated were in the hundreds of micromolar to millimolar concentrations which raises the question of what concentrations of volatile chemicals are plants able to detect. Most odorant binding proteins found in insects and animals have binding constants in the low micromolar range for the target analytes. So if these putative plant odorant binding proteins do have a role in chemical sensing further practical experiments are needed and these need to be discussed. The data are not enough to indicate that these putative proteins identified have relevant functions in chemical sensing in plants.

  5. Version published to 10.7554/elife.66741 on eLife
  6. Version published to 10.1101/2021.03.02.433599v1 on bioRxiv