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Plant roots: Understanding structure and function in an ocean of complexity

Article  in  Annals of Botany · October 2016

DOI: 10.1093/aob/mcw192

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 Annals of Botany 118: 555–559, 2016
doi:10.1093/aob/mcw192, available online at www.aob.oxfordjournals.org

PREFACE: PART OF A SPECIAL ISSUE ON ROOT BIOLOGY

Plant roots: understanding structure and function in an ocean of complexity

Peter R. Ryan1,*, Emmanuel Delhaize1, Michelle Watt2 and Alan E. Richardson1
1
CSIRO Agriculture and Food, GPO Box 1600, Canberra, ACT 2601, Australia and 2Plant Sciences Institute, Bio and Geo
Sciences, Forschungszentrum Jülich GmbH, 52425 Jülich, Germany
*For correspondence. E-mail [email protected]

Received: 3 August 2016 Returned for revision: 6 August 2016 Accepted: 19 August 2016

 Background The structure and function of plant roots and their interactions with soil are exciting scientific fron-
tiers that will ultimately reveal much about our natural systems, global water and mineral and carbon cycles, and
help secure food supplies into the future. This Special Issue presents a collection of papers that address topics at the
forefront of our understanding of root biology.
 Scope These papers investigate how roots cope with drought, nutrient deficiencies, toxicities and soil compaction
as well as the interactions that roots have with soil microorganisms. Roots of model plant species, annual crops and
perennial species are studied in short-term experiments through to multi-year trials. Spatial scales range from the
gene up to farming systems and nutrient cycling. The diverse, integrated approaches described by these studies en-
compass root genetics as applied to soil management, as well as documenting the signalling processes occurring be-
tween roots and shoots and between roots and soil.
 Conclusions This Special Issue on roots presents invited reviews and research papers covering a span of topics
ranging from fundamental aspects of anatomy, growth and water uptake to roots in crop and pasture systems.
Understanding root structure and function and adaptation to the abiotic and biotic stresses encountered in field con-
ditions is important for sustainable agricultural production and better management of natural systems.

Key words: Rhizosphere, water, nutrients, perennial, signals, plant-microbe interactions, abiotic stress, growth.

INTRODUCTION and how they influence shoots and seed production, but to do
so in the context of the surrounding soil and biomes. In one
It is staggering how much we have learnt about the natural sense the issues hampering the study of blue whales and plant
world over recent decades. Much of the research progress in bi- roots are similar – they are both surrounded by an ocean of
ological systems has been driven by new technologies that en- complexity with enormous spatial and temporal variability.
able them to be investigated in greater detail at every scale: Nevertheless, the mysteries surrounding roots are gradually be-
from genomes, transcriptomes and metabolomes at the subcel- ing unravelled, as described by the articles presented in this
lular level, all the way up to fields, forests and ecosystems. Yet Special Issue. The genetic and phenotypic variability of roots
the deeper we probe, the greater our surprise at the gaps that re- remains to be fully exploited by breeders to benefit agricultural
main. This is as true for the commonplace weeds in our gardens productivity and sustain natural plant systems. Filling the
as it is for our iconic species. For instance, it is bewildering knowledge gaps in root research will bring opportunities for im-
how little is known about the blue whale (Balaenoptera muscu- proving food security and environmental sustainability.
lus), the largest animal that has ever lived on the planet and a
creature that still swims along the coastline of every continent
on Earth. Zoologists don’t know how long blue whales live for,
ROOTS AND WATER
how they communicate, nor much at all about their courtship
and reproduction. Equally bewildering for plant biologists are Drought is the major limitation to the growth of crops and the
the gaps in our knowledge about basic plant processes and their distribution of natural plant communities globally, and several
interactions with the environment, considering the critical role papers address the physics and physiology of water uptake by
plants play in the air we breathe, the food we eat and the fibres roots. Zarebanadkouki et al. (2016) remind us how little is
we use. Our understanding of roots, the ‘hidden half’ of plants known about basic aspects of water uptake. Hydraulic conduc-
(Eshel and Beeckman, 2013), is even more rudimentary than tance is a critical parameter for understanding water uptake by
that of shoots or flowers. Much of the biology controlling roots’ roots, yet few models take into account the variation in conduc-
functions in anchorage, storage, resource acquisition and com- tance that is likely to occur along roots and radially within roots.
munication remains a mystery. Apart from specific root crops This uncertainty was examined by mapping the spatial variation
like carrot and cassava (Stein and Nothnagel, 1995; Nassar and of water uptake in lupin (Lupinus albus) roots. Using neutron ra-
Ortiz, 2007), below-ground traits are rarely considered by plant diography the authors demonstrate that water uptake varies sig-
breeders and dendrologists because roots are so difficult to ob- nificantly between different types of roots as well as along roots.
serve and study in situ. The pressing challenge for plant biolo- This information is useful for developing realistic models for
gists is not only to improve our understanding of root functions water uptake from soil. Pioneering work by Gardner (1960)
C The Author 2016. Published by Oxford University Press on behalf of the Annals of Botany Company.
V
All rights reserved. For Permissions, please email: [email protected]
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 556 Ryan et al. — Plant roots: understanding structure and function

considered the moisture gradients in soil immediately adjacent production. White clover (Trifolium repens) is one of the most
to roots, but a clear understanding of the behaviour of water at important forage species in temperate zones yet is prone to
that interface is still lacking. This topic was addressed by drought stress due to its relatively small and shallow root sys-
Carminati et al. (2016), who developed a biophysical model to tem. White clover also competes poorly for nutrients when in-
explain the changes that occur in the xylem water potential as cluded in swards with grasses. Nichols et al. (2016) describe
the soil dries. Their model provides a framework for estimating their strategies for improving the root structure of white clover
the water potential across the rhizosphere and for predicting by crosses to a range of Trifolium uniflorum accessions.
moisture levels directly adjacent to the root surface. Several characteristics of the backcross hybrids were altered,
Root hydraulic conductivity in a drying soil was also investi- including root depth and root length density. The results dem-
gated experimentally by Henry et al. (2016) using drought- onstrate that targeted breeding strategies can be used to alter
susceptible and drought-tolerant cultivars of rice (Oryza sativa). root architecture to improve pasture production. An important
Bleeding rates (sap exuded from a cut stem) were compared role of roots is to provide support and stability to the plant
with vapour pressure deficit and transpiration rates during diur- shoots. Dorval et al. (2016) examined how root architecture af-
nal and seasonal cycles. They show how changes in these envi- fects stability and anchorage in young Pinus pinaster trees.
ronmental factors affect root hydraulic conductivity and They identify several root shapes that are particularly beneficial
suggest a link between suberin content of roots and drought tol- on sandy soils and conclude that a large proportion of the an-
erance. Meng et al. (2016) investigated how rice plants balance chorage can be attributed to the distal region of the tap root and
the demand for water from the shoots with the supply of water associated laterals. In agro-forestry production systems, compe-
by the roots. They show that changes in water demand alter the tition between roots from different perennials could limit the
expression of aquaporins in the roots. Removing the shoots rap- productivity of either one or both species. This idea was tested
idly decreased the hydraulic conductance of the roots and de- in a mixed coffee (Coffea arabica)/tree (Erythrina poeppigi-
creased transcript levels of six aquaporin genes. These ana) plantation by Defrenet et al. (2016). This group monitored
responses were reduced if xylem tension was maintained after root biomass and fine-root density to 4 m depth in different
excision by quickly applying a vacuum to the cut stems. The parts of the plantation with contrasting light environments. No
authors propose that xylem water tension acts as a signal be- significant effects of the larger shading trees on the fine roots
tween shoots and roots to coordinate water supply with de- of coffee were found and the study concludes that coffee roots
mand. Aquaporin function was investigated in barley (Hordeum are very competitive in this system. Finally, Bastos et al.
vulgare) roots by Sharipova et al. (2016) with an immunochem- (2016) provide the first detailed anatomical study of roots from
ical approach. They applied abscisic acid (ABA) treatments to the woody vines collectively called lianas. Using traditional
wild-type plants and an ABA-deficient mutant and successfully techniques and X-ray microtomography analysis, they compare
linked local ABA concentrations with the abundance of aqua- and contrast mature roots from 14 species in the Paullinieae
porins and changes in root hydraulic conductivity. tribe (Sapidaceae) and highlight differences from known tissue
Many fundamental questions concerning how water moves anatomies in the stems of these species.
from the soil to the shoots remain to be answered. The studies Such studies on perennial roots are arguably at the forefront
mentioned above share the central objective of understanding of root biology and function, and constitute an exciting field for
how water movement is controlled by roots, but the scale of the root research in the future. Much of our knowledge on roots to
investigations varies widely, from analysis of the root–soil in- date has come from observations of annual, short-lived plants,
terface and specific transporter proteins on root-cell mem- and has been particularly focused upon the roots of relatively
branes, to total hydraulic conductivity. In situ measurements young plants. The roots of plants that live over several seasons,
using tracers showed fine spatial control of water flow along re-colonizing soil profiles year after year, decaying and inter-
roots that was influenced by age and soil moisture. This likely acting with microorganisms and cycling nutrients and water
reflects further levels of regulation. These studies confirm roles over years, are difficult to investigate but present opportunities
for hormones, protein transporters and cell-wall structure in wa- for many discoveries. Such discoveries have wide and impor-
ter uptake, indicating the necessity for complex signals to coor- tant implications for global productivity. For example, peren-
dinate these factors. nial biofuel crops are potentially more energy-efficient because
they don’t need to be re-sown annually. Forests, trees and pe-
rennial shrubs regulate water and carbon cycling to many
metres below ground, and while roots are critical to these pro-
PERENNIAL ROOT SYSTEMS
cesses very little detail is known about their regulatory roles.
Roots of some perennial species can pose additional hurdles to
researchers because of their size, depth and difficulty of manip-
ulation. These challenges are considered in a detailed review
RESPONSES TO ABIOTIC STRESSES
by Pierret et al. (2016) that explores the complex physiology of
deep roots, including the different functions they perform at Several papers examine how roots respond to abiotic stresses,
various depths. The authors critically examine popular models including nutritional limitations, elemental toxicities, waterlog-
describing the structures and functions of deep roots. They con- ging and physical constraints. Soil acidity affects more than
clude that most current models are supported by scant evidence 30 % of arable land and continues to limit agricultural produc-
and suggest priority areas for future research to improve these tivity globally. Aluminium and manganese toxicities are
models. Rooting depth is important for the perennial pastures largely responsible for poor plant growth but nutrient deficien-
so central to the grazing systems that support milk and meat cies also contribute. Many species have evolved strategies to

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 Ryan et al. — Plant roots: understanding structure and function 557

cope with these stresses, and Rao et al. (2016) comprehen- Phenotypic screens for single, abiotic soil constraints, such
sively review the adaptive changes in root structure and func- as those in the studies summarized above, can reveal the genetic
tion that provide protection from these hostile soils. They and physiological basis of tolerance mechanisms. Similar stud-
encourage further breeding strategies to select for additional ies have identified many new membrane transport proteins that
root traits. Lıska et al. (2016) demonstrate how exposure of regulate the uptake of nutrients and the exclusion of toxic ions
roots to air, or to toxic metals such as cadmium, influences the through specific root exudates (Schroeder et al., 2013). The
development of suberin lamella. Suberin is a wax-like cell-wall next step will be to combine these treatments and score perfor-
polymer that provides a barrier to the movement of water and mance with the multiple stresses encountered in the field. This
solutes. They find that suberin is preferentially deposited on will accelerate progress towards improving agricultural produc-
the side of the root exposed to these treatments, presumably as tion and provide management options for forestry and natural
a means of protecting the plant from these stresses. Metabolic systems (Rich and Watt, 2013).
responses to phosphorus deficiency in rice (O. sativa) were in-
vestigated by Zhu et al. (2016). This paper examines phospho-
rus recycling from roots to the shoots, where the phosphorus
supply is restricted, and reports that ethylene regulates this pro-
GROWTH AND DEVELOPMENT
cess. Raising ethylene concentrations in phosphorus-deficient
rice plants increased cell wall pectin content and the expression Several papers investigate root growth and development with
of the phosphate transporter OsPT2; both of these changes ac- mathematical models and by examining the mechanisms that
celerated phosphorus release from the root cell walls, which in- control growth. Le Deunff et al. (2016) surmise that root
creased phosphorus translocation to the shoots. Compaction is growth relies on a specific set of signals involving hormones,
another major soil constraint that affects root penetration and nutrients and carbon supply. They generated a fractal-based
final rooting depth. Popova et al. (2016) studied the effect of model for root development that accounts for specific interac-
soil strength on elongation rate and diameter of maize (Zea tions between ethylene levels, nitrogen availability and energy
mays) roots. Their paper describes how final root shape and supply. Pacheco-Escobedo et al. (2016) also adopted a mathe-
tortuosity in compacted soil results not only from mechanical matical approach to map the developmental zones at the root
deflections but also from tropic responses via touch stimuli. apices using a ‘multiple structural change’ algorithm. A spatial
Mechanical stress is also the topic of a study by De Zio et al. model was developed that predicted three main developmental
(2016). They examined roots of the woody perennial Populus regions they named the proliferation, transition and elongation
nigra and compared the anatomy, lignin content and hormone domains. These domains represent stages of differentiation, and
concentrations on the convex and concave sides of roots forced the position of the transition zone was confirmed with trans-
to turn a tight corner. Lignin content and xylem thickness in- genic Arabidopsis lines that expressed the green fluorescent
creased on the concave side whereas more lateral roots ap- protein at specific stages of the cell cycle. These domains are
peared on the convex side. Hormone analysis indicates that controlled by interacting regulatory networks of signals and
auxin and abscisic acid concentrations were likely to be re- transcription factors. Pacheco-Escobedo et al. (2016) further
sponsible for regulating these changes. Interestingly, the re- show that a transcription factor encoded by the MADS-box
sponses of roots to mechanical stress contrasts with the family gene XAANTAL1 (XAL1) affects the size of the prolifer-
modifications known to occur in the stems of poplar plants ation zone and critical length of dividing cells. This same
(Plomion et al., 2001). MADS-box gene was investigated by Garcıa-Cruz et al.
Waterlogging presents a number of physical and chemical (2016). They describe how the loss-of-function Arabidopsis
stresses to plants but the reduction in oxygen availability can mutant xal1 had altered expression of several key cell-cycle
limit growth and survival. Some species, such as alligator weed genes, disrupted tissue differentiation patterns and reduced cor-
(Alternanthera philoxeroides), are well adapted to flooded con- tical cell length. Reverse genetics approaches like this one will
ditions because they have evolved specific mechanisms to over- help to untangle the complex networks controlling root growth.
come this limitation, and consequently have become a major Cluster roots are specific root types that form in some species
threat to wetlands, rivers and irrigation systems around the in response to phosphorus deficiency. They are viewed as an ef-
world. Alligator weed is a perennial, growing vigorously and fective strategy for plants to extract phosphorus from soil pools
forming an intricate root system of adventitious roots that sus- not usually available to other plants. Cluster roots typically
pend in water. Ayi et al. (2016) investigated the adventitious comprise a region of densely arranged short secondary laterals
roots that develop on alligator weed in submerged conditions. thickly covered with root hairs. In addition to providing a large
They measured the oxygen gradients in the unstirred layers ad- surface area for absorbing nutrients, cluster roots exude protons,
jacent to these roots and provide evidence that they are capable organic anions and phosphatases to increase the concentration
of absorbing oxygen from the water. They also demonstrate of available phosphate in that region (Neumann and Martinoia,
that oxygen concentration within stem nodes having adventi- 2002). The efflux of citrate and malate from cluster roots is de-
tious roots increased compared with stem nodes without adven- pendent, in part, on the activity of phosphoenolpyruvate car-
titious roots, suggesting that oxygen may intimately regulate boxylase (PEPC). Shane et al. (2016) investigated the
their development, possibly helping to supply carbohydrate for regulation of PEPC in the cluster roots of white lupin (L. albus)
vigorous root growth. It remains to be shown whether the by monitoring the effect of light and sugar supply on organic
development of these adventitious roots offers alligator weed anion exudation. They report that PEPC activity in these tissues
greater capacity to absorb oxygen from water than similar roots is post-translationally regulated by the light-dependent, revers-
in other species. ible phosphorylation of the PEPC proteins. Their findings

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 558 Ryan et al. — Plant roots: understanding structure and function

demonstrate that sucrose translocated from source leaves down goal. The authors compare two cropping systems in Australia
to the roots influences the activity of this enzyme in sink and Denmark, where deep roots can benefit wheat yields by en-
tissues. abling access to stored soil water and nitrogen late in the sea-
son. They argue that the preceding crop, management during
the fallow period, and sowing date have a large influence on
PLANT–MICROBE INTERACTIONS subsequent wheat yields. While screens to optimize root sys-
tems should benefit productivity, the authors conclude that the
Signalling processes associated with root development and the
target traits need to be carefully matched with the local condi-
cross-talk between roots and soil microorganisms has emerged
tions and management practices. Screening methodologies are
as an exciting topic in plant biology. A paper by Lamont and
central to the contribution by Thomas et al. (2016). This project
Pérez-Fernandez (2016) describes how the emergence of the
scored canola (Brassica napus) varieties for shoot and root
cluster roots in three distinct species from different genera and
characters in the laboratory and in the field over three seasons.
geographic origin (Leucadendron salicifolium, Viminaria jun-
They conclude that primary root length and field performance
cea and Lupinus albus) was affected by inoculation with seven
were correlated with early vigour, which is more easily scored
different bacterial strains and nitrogen treatments. The paper re-
for in the shoots. However, they find that lateral root density
ports that six of the bacterial strains induced greater cluster root
was correlated with calcium and zinc concentrations in the
production than the aseptic controls. This response was not cor-
leaves, and these analyses could potentially be used as a surro-
related with the relative ability of these bacterial strains to pro-
gate screen for root traits. These papers illustrate the value of
duce indole-3-acetic acid, a hormone previously linked with
designing screens for root traits that match the field conditions
cluster root production. Microorganisms trigger other responses
where they need to function. By matching root and rhizosphere
in roots, and Koroney et al. (2016) examine how a pathogen
phenotypes with the soil, climate and regional management
can affect the composition of root exudates. They challenged
practices, root researchers will contribute more directly to the
potato (Solanum tuberosum) roots with an elicitor isolated from
productivity and efficiency gains needed for global food, water
Pectobacterium atrosepticum, a soil-borne pathogen of potato.
and land security.
They found that these inoculations altered the composition of
the galactose-containing compounds and arabinogalactan pro-
teins exuded from the root border cells of potato. They show CONCLUSIONS
that the in vitro growth rate of the pathogen depended on
whether it was exposed to exudates collected from induced or While the new tools afforded by biotechnology, computing
non-induced border cells. These results illustrate the dynamic power and satellite imagery have allowed unprecedented prog-
nature of the stimulus–response interactions that likely occur ress in root research, basic measurements remain a challenge.
continually between roots and the microbiome. Song et al. Phenotyping roots in situ is still a major obstacle. The intricate
(2016) contribute a further study on signalling in roots. In this communication between roots and microorganisms is emerging
paper, systemic acquired resistance (SAR) was induced in as another frontier in root research. Much has been achieved in
shoots of tobacco plants (Nicotiana benthamiana) by applica- laboratory-based studies, but it is clear that the shape and func-
tion of benzthiadiazole, and transmission of SAR between tion of roots grown in the field can be quite distinct from that of
neighbouring plants was subsequently shown to occur by root- those grown in pots or hydroponics. The challenge is not only
to-root transmission via a salicylic acid-mediated pathway. This to understand how roots function but to do so in soil with all its
was tested by challenging the adjoining plants with root physical, chemical and biological complexity. This is an excit-
(Pseudomonas syringae) and leaf (Ralstonia solanacearum) ing time to be involved in root research, but we need to ac-
pathogens and showing that the disease severity of the neigh- knowledge, with some humility, that our understanding of
bouring plants, not directly treated with benzthiadiazole, was organisms as commonplace as a weed or as grand as a blue
reduced. These three papers reveal some of the connections be- whale remains in its infancy.
tween roots and the wider soil microbiome and highlight their
involvement in elaborate communication pathways both within
and between plants. Understanding how roots interact and com- DEDICATION
municate with the soil microbiome through the release of exu- This Special Issue is dedicated to the memory of Michael
dates and other metabolites is a rapidly emerging area of Shane, the lead author of Shane et al. (2016), who sadly passed
research that offers new opportunities for plant protection and away shortly after this manuscript was accepted for publication.
growth promotion. Indeed, the root microbiome, which encom- Mike studied at the Carleton University in Ottawa before con-
passes root endophytes and microorganisms that colonize the tinuing his commitment to root research for many years at the
rhizoplane, rhizosphere and mycorrhizosphere, is now recog- University of Western Australia. The Editors of this Special
nized as being part of the ‘extended phenotype’ of the plant. Issue knew Mike and his excellent research on so many aspects
of root biology very well. Our thoughts and condolences are ex-
tended to Mike’s family, friends and many colleagues.
FARMING SYSTEMS
A long-term aim of much plant research is to identify root traits ACKNOWLEDGEMENTS
that can be exploited to improve agricultural production, and
Thorup-Kristensen and Kirkegaard (2016) emphasize in their We acknowledge the International Society of Root Research
review some of the practical considerations for achieving this for the ninth and most recent symposium entitled ‘Roots

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 Ryan et al. — Plant roots: understanding structure and function 559

Down Under: Belowground Solutions for Global Nichols SN, Hofmann RW, Williams WM, van Koten C. 2016. Rooting depth
Challenges’, held in Canberra, Australia, on 6–9 October and root depth distribution of Trifolium repens  T. uniflorum interspecific
hybrids. Annals of Botany 118: 699–710.
2015. This symposium provided a forum for root researchers Neumann G, Martinoia E. 2002. Cluster roots – an underground adaptation for
to share the latest results and ideas about the fundamentals survival in extreme environments. Trends in Plant Science 7: 162–167.
of how roots function and provided the stimulus for this Pacheco-Escobedo MA, Ivanov VB, Ransom-Rodrıguez I, et al. 2016.
Special Issue. Longitudinal zonation pattern in Arabidopsis root tip defined by a multiple
structural change algorithm. Annals of Botany 118: 763–776.
Pierret A, Maeght J-L, Clément C, Montoroi J-P, Hartmann C,
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