7. Ballaré, C.L.

(1999) Keeping up with the neighbours: phy-

proposed plant ocelli is weaker; and (iii) the changes in light intensity, orientation, or tochrome sensing and other signalling mechanisms.
idea of vision in higher plants not only is quality that photoreceptors (or the hypo- Trends Plant Sci. 4, 97–102

unsupported by facts, but also, and more thetical plant ocelli) may sense. 8. Karban, R. (2015) Plant Sensing and Communication, The
University of Chicago Press
importantly, is not necessary. 9. Van Loon, L.C. (2016) The intelligent behavior of plants.
Plants show finely tuned responses to an Trends Plant Sci. 21, 286–294

Baluška and Mancuso consider implausi- array of stimuli [8]. Plant vision is not nec- 10. Mabey, R. (2016) The Cabaret of Plants: Forty Thousand
Years of Plant Life and the Human Imagination, W.W.
ble that volatile communication or con- essary to account for the adaptive features Norton & Company
temporary horizontal gene transfer may that plants exhibit and that have allowed 11. Ahmad, M. (1999) Seeing the world in red and blue: insight
into plant vision and photoreceptors. Curr. Opin. Plant Biol.
account for leaf mimicry in B. trifoliolata them such immense evolutionary suc- 2, 230–235
‘because: (i) when the host tree is devoid cess. Of course, there are still some puz-
of leaves, the vine leaves adopt a normal zling phenomena, leaf mimicry among
(standard) morphology; and (ii) the vine them, that lack an explanation to date,
leaves mimic the closest leaves even if but currently there is no solid evidence
these are not part of the climbed host tree for the existence or function of plant ocelli
Letter
but belong to some nearby tree’ [1]. What in this regard. Plants are amazing organ- Plant Ocelli for
the first fact merely indicates is that when isms whose capabilities often defy human
there is no nearby leaf model (i.e., no preconceptions [9,10] and surely other Visually Guided Plant
source of whatever stimuli or elements), extraordinary features remain to be dis-
the vine does not change its appearance, covered. Challenging and creative ideas,
Behavior
by no means disproving a hypothetical as those discussed by Baluška and Man- Stefano Mancuso1,* and
mechanism for leaf mimicry. It is evident cuso, may be useful to this end. Nonethe-
Frantisek Baluška2
that the second fact (no contact needed less, scientists in this endeavor must be
for mimicry to occur) supports the idea of rigorous in avoiding overinterpretation of
In his recent commentary [1] on our con-
an airborne signal or vector that triggers evidence and unjustified beliefs that plant
ceptual paper related to plant ocelli [2],
the phenomenon at short distance; again, abilities should mirror those of animals.
Ernesto Gianoli expresses concerns
it says nothing for or against a particular Just as animals do not need to photosyn-
about the plausibility of plant vision via
mechanism for leaf mimicry. Host volatile thesize, plants do not need to see. Or, to
plant-specific ocelli. Gianoli is critical of
recognition has been considered a plau- be more precise, plants do not need to
vision-like processes in plants in general,
sible explanation for the observed leaf have eyes: some authors may interpret
and of plant ocelli in particular. Specifically,
mimicry [6]. that plants in fact ‘see’ due to their phyto-
he highlights the processes potentially
chrome- or cryptochrome-mediated per-
involved in leaf mimicry of the climbing
The leaf mimicry phenomenon is qualita- ception of light intensity, orientation, and
plant Boquila trifoliolata, for which he pre-
tively different from phototaxis and leaf quality [9,11].
fers other explanations, such as volatile
orientation. The latter phenomena involve
signaling and horizontal gene transfer on
relatively simple, quantitative changes in 1
Departamento de Biología, Universidad de La Serena, an ecological timescale [1]. We thank
the known function or behavior of a given Casilla 554 La Serena, Chile
Ernesto Gianoli for raising his concerns,
organ. For instance, changes in leaf orien- 2Departamento de Botánica, Universidad de Concepción,
but we remain convinced that the concept
tation following kin presence in Arabidop- Concepción, Chile
of plant ocelli is more convincing than are
sis involve perception of the red/far-red *Correspondence: egianoli@userena.cl (E. Gianoli).
the alternative explanations, particularly
light and blue light profiles [4], which are http://dx.doi.org/10.1016/j.tplants.2016.11.001
given that it is supported by experimental
known mechanisms of detection of neigh-
results and is the only realistic explanation
boring plants and elicitation of the shade- References
1. Baluška, F. and Mancuso, S. (2016) Vision in plants via of Boquila trifoliolata mimicry.
avoidance syndrome [7]. By contrast, to plant-specific ocelli? Trends Plant Sci. 21, 727–730
accomplish leaf mimicry, B. trifoliolata 2. Schuergers, N. et al. (2016) Cyanobacteria use micro- If vision had evolved in cyanobacteria and
optics to sense light direction. eLife 5, e12620
must produce dramatic changes in terms unicellular algae before the origin of higher
3. Gavelis, G.S. et al. (2015) Eye-like ocelloids are built from
of size, shape, color, orientation, petiole different endosymbiotically acquired components. Nature organisms [3–8], it is plausible that this
length, and vein conspicuousness, and 523, 204–207 ability has not been lost during evolution.
4. Crepy, M.A. and Casal, J.J. (2015) Photoreceptor-medi-
even develop spiny tips (Figure 1 and ated kin recognition in plants. New Phytol. 205, 329–338
In fact, it would be surprising to find that
[5]). Moreover, all of these changes must 5. Gianoli, E. and Carrasco-Urra, F. (2014) Leaf mimicry in a plants are not endowed with similar mech-
conform to a coherent, integrated pheno- climbing plant protects against herbivory. Curr. Biol. 24, anisms, especially given that this feature is
984–987
type. Such morphological complexity is 6. Trewavas, T. (2016) Plant intelligence: an overview. BioSci- preserved in multicellular algae, such as
highly unlikely to be driven by the simple ence 66, 542–551 Volvox [9]; in this instance, peripheral cells

Trends in Plant Science, January 2017, Vol. 22, No. 1 5


concentrate light to transmit to cells
deeper within the organism, which is simi-
lar to what is proposed to occur in higher
plants [9]. These peripheral cells in a Vol-
vox colony act as lenses [9], exactly as
suggested by Gottlieb Haberland in 1905
for plant leaf epidermis cells [10].
To mimic precisely complex objects such
as leaves, Boquila must be capable of
sensing parameters such as shape, dimen-
sion, and color [1,2,11]. In other words, it
must be able to perceive vectorial sensory
information. To do that, it would appear to
us that some kind of vision would be cru-
cial. In fact, chemical components, includ-
ing volatiles and RNA and/or DNA
molecules, cannot provide any vectorial
sensory information. Although we do not
dismiss the involvement of volatiles or other
chemicals [1,11], in our opinion, these have
only supportive roles. Of course, to elimi-
nate any doubt, relevant experiments,
which are not difficult to conceive, must
be performed. It will be necessary to ana-
lyze the light-transmission properties of
Boquila leaf epidermis and to determine
whether Boquila leaf mimicry continues to
operate similarly under different light quali-
ties or in complete darkness. Plant roots will
also prove to be relevant, because the
navigation of root tips appears to be visually
guided [12,13] and underground roots
directly sense stem-piped light to monitor
the aboveground light environment during
plant environmental adaptation [14].
It is important to be aware that the plant
ocelli concept was not originally proposed
due to some fanciful and overspeculative
ideas, but was based on the results of well-
designed experiments with leaf epidermis of
diverse plant species performed by Haber-
land [10,15] and later confirmed by Wager's
experiments [16]. Finally, as meritoriously
stated in two recent papers by Nilsson
and colleagues [7,17], any behavior and/
or movement that is based on directional
photoreception must be regarded as vision.
In this sense, phototropism and shade
avoidance are examples already available
of visually guided behavior in plants.
6 Trends in Plant Science, January 2017, Vol. 22, No. 1
1
University of Firenze, LINV, DISPAA, viale delle Idee 30,
Sesto Fiorentino, Florence, 50019, Italy
2
University of Bonn, IZMB, Kirschallee 1, 53115 Bonn,
Germany
*Correspondence: stefano.mancuso@unifi.it (S. Mancuso).
http://dx.doi.org/10.1016/j.tplants.2016.11.009
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optics to sense light direction. Elife 5, e12620
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different endosymbiotically acquired components. Nature
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984–987
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Visual Neurosci. 30, 5–20
Spotlight
Engineering Dual
Begomovirus-
Bemisia tabaci
Resistance in Plants
Syed Shan-e-Ali Zaidi,1
Rob W. Briddon,1 and
Shahid Mansoor1,*
The whitefly Bemisia tabaci is an
important pest of many economi-
cally important crops and the vector
of begomoviruses (family Geminivir-
idae). Recently, the expression of
insecticidal proteins and/or toxins
or double-stranded (ds)RNA homol-
ogous to B. tabaci genes has been
demonstrated to provide the plant
with protection against B. tabaci
and the viruses that it transmits.
Agricultural Pests
The whitefly (Hemiptera: Aleyrodidae)
Bemisia tabaci is considered to be one
of the most invasive organisms and has
been included in the list of the ‘100 of the
World's worst invasive alien species’i. It
occurs naturally throughout tropical and
subtropical regions of the world. However,
B. tabaci has spread globally, most prob-
ably through the movement of agricultural
products, and has emerged as one of the
most damaging agricultural pests in the
world within the past 20 years [1]. The
insect damages the plant both directly,
by sucking phloem sap, resulting in
stunted growth, early wilting, premature
defoliation, and, eventually, yield loss,
and indirectly, by the honeydew it
excretes, which promotes fungal growth
on leaves and fruit surfaces. Additionally,
B. tabaci transmits plant viruses. The most
important among these viruses are bego-
moviruses (family Geminiviridae), although
B. tabaci is also a vector of criniviruses,
ipomoviruses, torradoviruses, and some
carlaviruses. Begomoviruses are the most
widespread plant viruses and cause dev-
astating yield losses to many economically
important crops, such as cotton, cassava,
beans, tomato, and cucurbits [2]. Collec-
tively, B. tabaci and begomoviruses are a
major threat to global agriculture and food
security.
Resistance Strategies
Since the severe outbreaks of B. tabaci and
begomoviruses during the late 20th cen-
tury, scientists from diverse fields have been