Plant Physiology 132:1779-1780 (2003)
© 2003 American Society of Plant Biologists
THE HOT AND THE CLASSIC
CIRCUMNUTATION
Time-lapse measurements of rapidly elongating plant organs reveal that the
growing tips of most organs, including roots, shoots, and coleoptiles, grow
helically about the plumbline (Johnsson,
1985 ). This month's "The Hot and the Classic" examines
some recent developments in our understanding of these poorly understood
circumnutatory movements.
Agricultural Importance of Circumnutation
Although circumnutatory movements are of obvious use to twining plants
seeking mechanical support, in many cases the movements appear to serve no
useful purpose. Many researchers have regarded them simply as oddities of
plant growth or perhaps an outward manifestation of some important processes
involved in the elongation of plant organs. Although there have been
occasional suggestions in the literature that circumnutation may aid
underground organs in soil penetration (e.g.
Fisher, 1964), this idea has
recently gained experimental confirmation in a study of paddy rice (Oryza
sativa) varieties (Inoue et al.,
1999). Although rice, an aquatic plant in origin, must have
evolved to acquire traits for securing seedling establishment under flooded
conditions, most modern varieties fail to become established under such
conditions. Inoue et al.
(1999) demonstrated that
varietal differences in seedling-establishment percentage were attributable
not to seminal root elongation rate or apparent weight of the seed in water,
but to differences in the penetrating ability of the seminal root into soil.
To examine whether root tip circumnutation could have been a facilitator of
soil penetration by the root, Inoue et al.
(1999) performed a spectrum
analysis of the root tip rotations of various varieties of rice seedlings.
Those seedlings that circumnutated with a frequency of 2 to 3.4 cycles per day
showed the highest seedling-establishment percentage. From these results, it
appears that root tip rotations with large spiral angles are more effective in
allowing the root tip to penetrate flooded or very soft soil.
A Role for Gravity Revisited
Charles Darwin and his son Francis suggested that circumnutatory movements
were mediated by an endogenous oscillator
(Darwin and Darwin, 1880). A
later school that attracted some adherents envisaged nutatory movements as
being a continuous series of over-compensatory responses of the plant to the
changing orientation of the its gravisensory apparatus relative of the Earth's
gravity vector (see Israelsson and
Johnsson, 1967). Part of the attraction of this gravitropic model
stemmed from the observation that the percentage of seedlings exhibiting
nutation is greatly enhanced by brief gravitropic stimulation. Experiments
performed under conditions of microgravity aboard the Spacelab, however,
revealed that gravity is an absolute requirement neither for the initiation
nor the continuation of circumnutatory movements in Helianthus annuus
hypocotyls (Brown, 1993). Thus,
the prevailing opinion once again became that circumnutatory movements are
endogenously regulated.
More recent experiments by Hatakeda et al.
(2003) emphasize that that
role of graviresponsiveness in amplifying circumnutational movements is not
trivial. These authors examined the nutational movements of a number of
gravitropically impaired Arabidopsis mutants. The inflorescences of wild-type
Arabidopsis showed relatively large circular movements. The pgm-1
mutant, which is defective in starch synthesis, showed reduced circumnutation.
Even more seriously affected were two mutants that were defective in
endodermal cell differentiation. Circumnutation also was not apparent in the
auxin-resistant axr2–1 mutant. It is important to emphasize,
however, that these agravitropic mutants did show nodding movements just not
the broad sweeping movements typical of circumnutation.
The Role of Auxin
It is apparent that circumnutation is linked to the movement of indolyl,3,
acetic acid (IAA). Indeed, there is a strong temporal correspondence between
circumnutation and the transport of auxin in both Triticum aestivum
coleoptiles (Arnal, 1953) and
Phaseolus vulgaris hypocotyls
(Heathcote, 1965); the point
of maximum curvature of the organs migrates basipetally during nutation at
approximately the same rate as the basipetal transport of IAA. The auxin
transport inhibitor naphthylphthalamic acid (NPA) has been found to abolish
the nutatory movements in Pisum sativum stems
(Britz and Galston, 1983).
Classic experiments demonstrated that the nutations of grass coleoptiles cease
following decapitation of the apex, the site of auxin release, or following
removal of the seed, the source of the bound auxin released in the apec.
Nutatory movements can be reawakened by the application of agar blocks
containing diffusible auxin to the cut surface
(Joerrens, 1959;
Anker, 1972;
Britz and Galston, 1983). These
findings indicate that oscillations in IAA synthesis or release are not
responsible for the movements and, more generally, that the apex is not the
site of the oscillator. Although these studies do indicate a role for IAA in
nutation, it would be a mistake simply to assume that if auxin is present,
then nutation will follow. Indeed, Anker
(1972) found that the feeding
of free IAA to the transpiration stream of decapitated oat coleoptiles failed
to restore nutation: the mere presence of free IAA is in itself insufficient
to elicit nutatory movements. Rather, nutatory movements appear to depend on
the natural polar movement of IAA through the plant.
Ionic Changes during Circumnutation
Circumutatory movements are caused by spirally propagating changes in the
extension rate of the organs' elongation (motor) zones
(Berg and Peacock, 1992).
Changes in K+ distribution underlie the nutatory movements of
Phaseolus vulgaris shoots (Badot
et al., 1990). These data are supported by pharmacological studies
that have shown that tetrethylammonium (TEA), a well-known K+
channel antagonist, increases the period of the nutatory movements of
Phaseolus shoots without affecting their elongation rate.
Li+ ions also inhibit circumnutation
(Millet et al., 1978;
Zachariessen and Johnsson,
1988). Although the pharmacology of Li is unclear, Li is a
well-known inhibitor of phosphoinositide turnover
(Gillaspy et al., 1995). In
such cases, the effects of Li+ can be reversed by the addition of
much lower concentrations of myoinositol. Given that phosphoinositide turnover
and intracellular Ca2+ release often give rise to
propagating Ca2+ waves, it would be interesting to
determine whether the effects of Li+ on circumnutatory movements
can also be reversed by myoinositol.
Oscillations in H+ and Ca2+ fluxes in the
elongation zone of Zea mays roots have been linked to circumnutation
(Shabala and Newman, 1997a),
and these authors have proposed a new model of circumnutation
(Shabala and Newman, 1997b).
The hypothesis supposes that a lowered growth rate on one side of a root could
occur in response to a local stimulus. This inhibition of growth is proposed
to propagate in opposite directions and at different speeds from the site of
initial stimulation, and to circumnavigate the circumference of the root.
Peter V. Minorsky
Department of Natural Sciences Mercy College Dobbs Ferry, NY
10522
FOOTNOTES
www.plantphysiol.org/cgi/doi/10.1104/pp.900085.
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