INSIGHTS | PERSPECTIVES
sciencemag.org SCIENCEGRAPHIC: N. DESAI/SCIENCEBy Ricardo F. H. Giehl and
Nicolaus von Wirén
A
s sessile organisms, plants rely on
their roots to acquire sufficient water
and nutrients from the soil. Making
the right choice about where to de-
ploy new roots can determine sur-
vival, especially when soil resources
are scarce and unevenly distributed. Re-
cently, it was discovered that plant roots can
respond to gradients of soil moisture by fa-
voring the formation of lateral roots toward
sites with available water ( 1 ). On page 1407
of this issue, Orosa-Puente et al. ( 2 ) show
how growth along an air-water interface in
the soil triggers asymmetric activation of a
signaling module coordinated by the plant
hormone auxin that biases lateral root ini-
tiation to the side in contact with water.
These findings demonstrate how spa-
tial environmental cues determine or-
gan formation in higher plants.
The ability to generate new roots
postembryonically confers plants a
high degree of developmental plas-
ticity. The formation of lateral roots
starts deep in the parental root tissue.
There, a specific number of cells of
the pericycle, the tissue that delimits
the root vasculature, are “primed” as
lateral root founder cells at periodic
intervals ( 3 ). Rather than progressing
continuously, the initiation of lateral
roots from primed pericycle cells can
be stimulated or arrested at any de-
velopmental stage ( 4 ), allowing roots
to adjust the number and spacing of
lateral roots to the prevailing envi-
ronmental conditions. This plastic-
ity offers plants the opportunity to
efficiently colonize regions of high
resource availability, as long as root
sensing mechanisms can precisely lo-
cate these sites.
In many plant species, low water
availability can stimulate root expan-
sion and steeper growth angles to
improve water uptake from deeper
soil layers ( 5 , 6 ). In soils that are not
completely dry or flooded, an air-
water interface develops between soil
particles (see the figure). At this microscale,
variations in water availability trigger ab-
scisic acid–dependent hydrotropic growth
to differentially modulate cell elongation,
allowing roots to bend toward water ( 7 , 8 ).
Additionally, tissue patterning is altered
when roots are exposed to differential wa-
ter availability on either side of the root.
This adaptive response, termed hydropat-
terning, induces the formation of root hairs
and aerenchyma (plant tissues containing
enlarged gas-filled intercellular spaces) in
the air-exposed side of roots, while posi-
tioning more lateral roots on the side that
has direct contact with water ( 1 ). Although
local water availability induces auxin bio-
synthesis and signaling ( 1 ), it has remained
unknown how these changes are translated
into asymmetrical lateral root formation
across the root axis.Orosa-Puente et al. found that muta-
tions in the transcription factor AUXIN
RESPONSE FACTOR 7 (ARF7), a key regu-
lator of lateral root initiation ( 9 ), impaired
the ability of plants to bias root branching
toward moisture. Although LATERAL OR-
GAN BOUNDARIES-DOMAIN 16 (LBD16),
a downstream target of ARF7, accumulates
preferentially in lateral root founder cells
on the water-exposed side, ARF7 is evenly
expressed around the circumferential axis of
the root. However, ARF7 can be posttransla-
tionally modified with small ubiquitin modi-
fier (SUMO). Arabidopsis plants lacking the
SUMO proteases OVERLY TOLERANT TO
SALT 1 (OTS1) and OTS2 ( 10 ), which promote
deconjugation of SUMO from ARF7, exhibit
a hydropatterning defect akin to ARF7 mu-
tants. Intriguingly, SUMOylation does not
affect the universal function of ARF7 to pro-
mote lateral root initiation but instead
affects its capability to regulate the
root branching pattern in response to
water. ARF proteins can be inactivated
by INDOLE-3-ACETIC ACID–INDUC-
IBLE (IAA) proteins in an auxin-de-
pendent manner ( 11 ). This is also the
case for ARF7, the DNA-binding activ-
ity of which is controlled by IAA3 and
IAA14 at different stages of lateral root
development ( 12 , 13 ). Orosa-Puente
et al. identified that SUMOylation is
specifically required for ARF7 recruit-
ment and inactivation by IAA3 but is
dispensable for the interaction with
IAA14. These findings provide insights
into how an environmental cue can
fine-tune the function of common
regulators of development to induce
specific phenotypic plasticity.
Hydropatterning is conserved in
many plant species and targets early
stages of lateral root development,
such as the positioning of founder cells
along the main root axis ( 1 ). Develop-
mental competence for hydropattern-
ing is largely limited to the root zone
undergoing active growth and is lost
as cells mature ( 14 ). This has led to
the hypothesis that water gradients
are sensed near the root tip, leaving a
positional imprint that triggers lateral
root initiation further up in the root.
In the growing root tip, cell expansion
builds up a water potential gradient
that increases hydraulic conductiv-PLANT BIOLOGY
Hydropatterning—how roots test the waters
Local water cues modulate auxin signaling to instruct root developmental decisions
Department of Physiology and Cell Biology, Leibniz
Institute of Plant Genetics and Crop Plant
Research (IPK), 06466 Gatersleben, Germany.
Email: [email protected]
Root hairSUMOPrimed
pericycle cellPericycle cell
GravityAir contact Water contactLateral rootsSoil particleIAA3
ARF7LBD16IAA3
ARF7LBD16Lateral root
initiation1358 21 DECEMBER 2018 • VOL 362 ISSUE 6421
Shaped by water
Where there are small-scale differences in water availability
around soil particles, water potential gradients are sensed in roots
(red cells). Hydrotropism guides roots towards water, whereas
hydropatterning alters the distribution of root hairs and lateral
roots along the root circumference (not to scale). ARF7-dependent
asymmetric LBD16 expression triggers lateral root initiation on the
side in contact with water.Published by AAASon December 20, 2018^http://science.sciencemag.org/Downloaded from