Professional Documents
Culture Documents
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Hidden Branches:
Developments in Root
System Architecture
Karen S. Osmont, Richard Sibout,
and Christian S. Hardtke
Department of Plant Molecular Biology, University of Lausanne, CH-1015 Lausanne,
Switzerland; email: karen.osmont@unil.ch, richard.sibout@unil.ch,
christian.hardtke@unil.ch
Key Words
Abstract
The root system is fundamentally important for plant growth and
survival because of its role in water and nutrient uptake. Therefore,
plants rely on modulation of root system architecture (RSA) to respond to a changing soil environment. Although RSA is a highly
plastic trait and varies both between and among species, the basic
root system morphology and its plasticity are controlled by inherent
genetic factors. These mediate the modication of RSA, mostly at
the level of root branching, in response to a suite of biotic and abiotic factors. Recent progress in the understanding of the molecular
basis of these responses suggests that they largely feed through hormone homeostasis and signaling pathways. Novel factors implicated
in the regulation of RSA in response to the myriad endogenous and
exogenous signals are also increasingly isolated through alternative
approaches such as quantitative trait locus analysis.
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Contents
Root system
architecture (RSA):
the threedimensional
structure of the root
system, including the
primary root, branch
roots, and root hairs
LR: lateral root
Adventitious roots:
roots that emerge
from shoot
structures
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INTRODUCTION . . . . . . . . . . . . . . . . . 94
The Morphological Diversity of
Root Systems . . . . . . . . . . . . . . . . . 95
THE DEVELOPMENTAL
PLASTICITY OF ROOT
BRANCHING: RESPONSE
TO EXOGENOUS
FACTORS . . . . . . . . . . . . . . . . . . . . . . . 96
The Molecular Basis of Root
System Response to
Nitrogen . . . . . . . . . . . . . . . . . . . . . . 96
The Molecular Basis of Root
System Response to
Phosphate. . . . . . . . . . . . . . . . . . . . . 97
Other Nutrients and Exogenous
Abiotic Factors Modulating
Root Branching . . . . . . . . . . . . . . . 97
ENDOGENOUS REGULATORS
OF ROOT SYSTEM
ARCHITECTURE: THE ROLE
OF PHYTOHORMONES . . . . . . . 98
Auxin . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98
Cytokinins . . . . . . . . . . . . . . . . . . . . . . . 99
Ethylene . . . . . . . . . . . . . . . . . . . . . . . . . 99
Gibberellins . . . . . . . . . . . . . . . . . . . . . . 99
Abscisic Acid . . . . . . . . . . . . . . . . . . . . . 99
Brassinosteroids . . . . . . . . . . . . . . . . . . 100
MODULATION OF ROOT
SYSTEM ARCHITECTURE BY
BIOTIC FACTORS . . . . . . . . . . . . .
Root System Architecture Changes
Triggered by Interaction with
Mycorrhizae . . . . . . . . . . . . . . . . . .
Nodulation . . . . . . . . . . . . . . . . . . . . . .
ROOT MERISTEM
FORMATION . . . . . . . . . . . . . . . . . . .
Cell Cycle Control of Lateral
Root Initiation . . . . . . . . . . . . . . . .
Making and Maintaining
Root Meristems . . . . . . . . . . . . . . .
New Protagonists in Lateral
Root Formation . . . . . . . . . . . . . . .
Regulators of Adventitious
Root Formation . . . . . . . . . . . . . . .
ALTERNATIVE APPROACHES
TO STUDY ROOT
BRANCHING . . . . . . . . . . . . . . . . . . .
Microarray and Proteomics
Analyses of Root Branching . . . .
Isolation of Modiers of Root
System Architecture by
Quantitative Trait Locus
Analyses . . . . . . . . . . . . . . . . . . . . . .
CONCLUSIONS . . . . . . . . . . . . . . . . . . .
INTRODUCTION
The root system primarily functions to acquire essential macro- and micronutrients and
water from the soil, and to provide anchorage.
It also participates in secondary functions, including, for example, photoassimilate storage,
phytohormone synthesis, or clonal propagation. During evolution, root organization has
gradually progressed from very simple, such
as rhizomes, to highly hierarchical, including
specialized tissues (12). This elaboration was
likely driven by the fact that the root system
is instrumental in facing major constraints to
plant growth and reproductive success: the
availability of nutrients and water, and the
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101
101
101
101
102
102
103
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103
104
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Figure 1
(a) Schematic representation of a typical allorhizic root system architecture as found in most dicotyledons,
exemplied by Arabidopsis, in 5-day-old and 12-day-old seedlings. Root hairs are not represented. PR,
primary root; LR, lateral root. (b) Schematic representation of a typical secondary homorhizic root
system architecture as found in most monocotyledons, exemplied by rice, in 7-day-old and 14-day-old
seedlings. Root hairs are not represented. PR, primary root; LR, lateral root; CR, crown root.
www.annualreviews.org Root System Architecture and Development
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THE DEVELOPMENTAL
PLASTICITY OF ROOT
BRANCHING: RESPONSE
TO EXOGENOUS FACTORS
RSA is inuenced by numerous biotic and
abiotic factors that make up the heterogeneous composition of the soil environment.
Thus, RSA is a highly plastic trait, meaning that genotypically identical plants can
heavily differ in RSA, depending on their
macro- and microenvironment. Although this
plasticity is well documented, the underlying molecular mechanisms are poorly understood. However, an increasing number of mutant studies in Arabidopsis start to address this
issue. For instance, one recent study examined
LR formation as a function of water availability. Indeed, lateral root primordia emergence is repressed when water becomes limiting, and this response requires abscisic acid
(ABA) and the LATERAL ROOT DEVELOPMENT2 gene (23). Apart from water, the
other most important abiotic factor for root
system growth is nutrient availability (32, 72).
Among the different nutrients, the abundance
of the two growth-limiting macronutrients,
nitrogen (N) and phosphorus (P), exerts the
greatest effect on RSA.
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situation is different in the more heterogeneous soil environment, where nutrients are
often unequally distributed. Indeed, localized
zones of high N concentration promote rather
than suppress LR growth (32). Therefore, LR
growth is systemically inhibited in response to
globally high levels of N, but locally induced
in response to N-rich patches. An important component in the latter response is the
nitrate-inducible Arabidopsis MADS box transcription factor NITRATE-REGULATED1
(ANR1) (118). In plants with decreased ANR1
activity, LRs do not proliferate in response to
nitrate-rich zones. However, systemic inhibition of LR growth is still maintained, suggesting that ANR1 exclusively mediates localized
responses to N.
Conceivably, N sensing and thereby root
branching are also affected by N transport.
In particular, the Arabidopsis NRT2 family
of transporter-like proteins is required for
HATS (42). One of its members, NRT2.1, was
recently implicated in LR initiation (68, 96).
Lateral root initiation is strongly repressed in
Arabidopsis by a high external carbon to nitrogen source ratio, and this response is abolished
in the lin1 mutant (79), which is defective in
NRT2.1 (68).
Another natural N source that strongly
inuences RSA is glutamate, which results
from the breakdown of organic matter.
L-glutamate-treated seedlings have a shorter,
more branched root system, and this response
is strain-dependent (113). Finally, nitric oxide is required for LR primordia formation in
tomato (22).
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ENDOGENOUS REGULATORS
OF ROOT SYSTEM
ARCHITECTURE: THE ROLE
OF PHYTOHORMONES
In addition to exogenous factors, several endogenous molecules are pivotal determinants
of RSA. For instance, vitamin C antagonizes the effects of N and sugar in LR
growth (91). Also, root growth is perturbed
in the rsr4 (reduced sugar response 4) mutant,
which requires vitamin B6 supplementation
for normal development (112). However, the
most important endogenous modulators of
root system development are the different
phytohormones.
The bulk of genetic and physiological
evidence suggests that nutrient status and
availability and other abiotic factors trigger changes in RSA by modulating hormone
homeostasis and/or signaling (44, 77). This
notion is supported by the observation that
responsiveness to certain abiotic factors is
lost if a certain hormone response pathway is
no longer fully functional. For instance, mutants in the auxin transport mediator AXR4
(28) are unable to respond to local N-rich
zones (119). Also, the systemic inhibition
of LR formation in high N conditions is
abolished in the ABA-insensitive mutant abi4
(104). Thus, auxin might mediate localized
responses to N, whereas ABA mediates systemic responses. Further, suboptimal sulfate
promotes root system growth by modulat98
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Auxin
The minor active endogenous auxin indole3-butyric acid is an efcient promoter of adventitious root formation and commonly used
as such in horticulture. However, the more
abundant IAA appears to be most important
for RSA in planta. Generally, IAA promotes
LR development, for instance when applied
exogenously (63, 64). Few exceptions to this
rule have been observed [for example, exogenous IAA application does not promote LR
formation in fern (55)]. Importantly, auxin is
necessary for all stages of lateral root development, i.e., initiation, emergence, and growth
(15, 16). In Arabidopsis, acropetal auxin transport from young aerial tissues into the primary root triggers lateral root formation by
promoting cell division of pericycle cells adjacent to xylem vessels (16). Basipetal auxin
transport in the root tip also appears to inuence LR emergence, despite the fact that LRs
emerge relatively far from root tips (16). The
precise site of LR initiation is probably more
a consequence of auxin transport than of de
novo auxin synthesis, although data to determine when and why a lateral root is initiated
in a certain position along a primary root are
lacking (3).
Genetic studies have conrmed the predominant role of auxin in LR formation.
For instance, mutants or transgenic lines
with elevated auxin biosynthesis display signicantly increased root branching (10, 60).
Consistently, mutants with low auxin content or impaired auxin signaling have a very
short, poorly branched root system (17), also
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conrming the requirement of auxin for primary root growth. However, overall auxin
content is not always positively correlated
with LR number. For instance, some mutants
with fewer LRs have elevated rather than decreased auxin levels, but are impaired in auxin
signaling (57). Nevertheless, as expected, mutants impaired in root polar auxin transport
are affected in LR development (51), and the
same is true for auxin signaling pathway mutants. For instance, the gain-of-function solitary root (slr) mutant, which carries a stabilizing mutation in the IAA14 negative regulator
of auxin signaling, displays decient early LR
primordium formation because cell division
is not maintained in the pericycle (41). Similarly, the gain-of-function mutant massugu2
(msg2), defective in IAA19, displays a signicantly decreased LR number. IAA19 inhibits
the activity of the auxin response factor (ARF)
NON-PHOTOTROPIC HYPOCOTYL 4
(NPH4)/ARF7, a positive regulator of
LR formation (110). In summary, both
auxin transport and signaling strongly inuence RSA, but, because of the inherent interdependency of these two processes
(65), their individual impact is difcult to
evaluate.
Ethylene
Cytokinins
Gibberellins
CK: cytokinin
GA: gibberellic acid
Abscisic Acid
Recently, ABA was also implicated in root system development because exogenous ABA application inhibits primary and lateral root development in Arabidopsis (7, 25). ABA action
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BR: brassinosteroids
in LR development is thought to be auxinindependent (25), but is modulated by nutrient availability (104). Interestingly, in rice
ABA stimulates rather than suppresses LR formation from primary roots (18). However,
whether this is a common feature of monocotyledons remains to be determined. Interaction between IAA and ABA has been also proposed, because some mutants with pleiotropic
defects in ABA responses in roots are also
impaired in auxin-mediated LR development
(11).
Brassinosteroids
Brassinosteroids (BRs) are abundant in shoots,
but have also been detected in substantial
amounts in roots of maize and tomato (117).
Indeed, gene expression studies suggest that
BRs are synthesized in roots, albeit at lower
levels than in shoots (59). Like auxin, BRs
promote primary root growth at low concentrations, but are inhibitory at higher con100
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MODULATION OF ROOT
SYSTEM ARCHITECTURE BY
BIOTIC FACTORS
RSA is not only inuenced by abiotic factors, but also by a range of biotic factors. Notably, in the wild, plant roots are in contact
with saprophytic and pathogenic microorganisms, which can drastically change RSA. For
example, after petunia is infected by specic
Ralstonia solanacearum strains, LR elongation
is inhibited, but new lateral roots with abnormal morphology are induced (120). Most
frequently, however, changes in RSA are triggered by symbiotic interactions. Unfortunately, the best-characterized plant model system, Arabidopsis thaliana, does not form root
symbioses and thus cannot be used to address questions of plant-symbiont interactions
and their impact on RSA. Nevertheless, an
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Nodulation
The second most important symbiosis of plant
roots is their association with N-xing bacteria in legumes, a process termed nodulation.
Nodules and LRs share some common fea-
tures. For instance, both organs form adjacent to xylem poles, develop meristems, and
break cell layers to emerge. In support of this
idea, the lateral root organ-defective mutant of
Medicago truncatula initiates both nodule and
LR formation, but does not complete either
process. Moreover, nodule formation shares
common molecular processes with LR development (24, 50).
Dichotomous:
branching of a
meristem into direct,
nearly equivalent
branches
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Thus, despite their obvious importance, it appears that cell cycle genes are not the primary
determinants of LR initiation.
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Regulators of Adventitious
Root Formation
As compared to LR formation, little is known
about the molecular basis of adventitious root
formation. In part, this might be due to the
rare occurrence of adventitious roots in the
early stages of normal Arabidopsis development. Although it is conceivable that the same
principal mechanisms as in LR formation are
at work, some signicant variation could be
expected, mainly because adventitious roots
generally form from differentiated stem tissues rather than from within other roots. Nevertheless, auxin signaling again appears to be
limiting for adventitious root formation in
Arabidopsis (105), a notion that is supported
by a recent study of a rice mutant, crown rootless1 (crl1).
CRL1 is necessary for crown root initiation
(56). However, crl1 defects can be overcome
by auxin treatment, suggesting that CRL1 acts
upstream of the auxin stimulus. Neverthe-
ALTERNATIVE APPROACHES
TO STUDY ROOT BRANCHING
Genetic redundancy generally limits the applicability of mutant analysis for the molecular genetic dissection of root branching in
Arabidopsis. Thus, alternative approaches are
a welcome complement to the described physiological and standard genetic techniques.
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QTL: quantative
trait locus
Figure 2
Root morphologies of different Arabidopsis thaliana wild accessions. Root system architecture of different
accessions at young stage grown in identical tissue culture conditions.
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CONCLUSIONS
Recent advances through forward- and
reverse-genetic approaches conrm the major
role of hormones, especially auxin, in LR initiation and development. An emerging theme
from these studies is the idea that most environmental responses of RSA are mediated
by modulating hormone homeostasis or signaling pathways. Novel insights in this process also surface from alternative approaches
to understand RSA, notably QTL analysis of
natural genetic variation. Also, other systems
and models are being increasingly exploited
to understand fully the variation and conservation of mechanisms underlying root growth
and RSA.
However, despite the recent efforts and
progress in understanding the molecular cues
involved in LR development, root branching, and RSA modulation, many unanswered
questions remain. For example, many factors involved in initiating, patterning, and
maintaining root meristems have been isolated in Arabidopsis. Most of these have been
dened for their requirement in primary root
development. Although recent evidence suggests that some of the pivotal factors have an
equivalent role in LR development, it remains
to be seen whether this is a general rule. For
example, the MONOPTEROS (MP) gene is
absolutely required for primary root formation in embryogenesis. However, mp loss-offunction mutants can form perfectly normal
adventitious roots (95). Does this mean that
homologous redundant factors take over MP s
role in different contexts (45), or is it an indication for an altogether alternative pathway
of adventitious root formation in Arabidopsis?
Many issues that are central to RSA have so
far not been elaborated on at the molecular
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SUMMARY POINTS
1. Although RSA is highly diverse, angiosperm root systems can be broadly classied into allorhizic, as in most dicotyledons, or secondary homorhizic, as in most
monocotyledons.
2. Despite the fact that RSA is a highly plastic trait and thus is difcult to study, several
molecular factors controlling root system morphology have been identied.
3. Although it is well established that RSA and root growth are strongly affected by the
nutrient status of the soil, the molecular mechanisms mediating root system responses
to nutrients are just beginning to be understood.
4. Almost all known plant hormones affect RSA, including auxin, CK, ethylene, BR,
ABA, and GA. However, recent evidence suggests that signicant interactions occur
between these hormone pathways to regulate root system growth. Moreover, it appears that hormones mediate root developmental responses to both biotic and abiotic
stresses downstream of the respective stimuli.
5. The auxin signaling pathway appears to be particularly important in mediating environmental responses of RSA.
6. Physiological data and recent molecular evidence suggest that symbiont establishment
shares common processes with LR development and strongly modulates RSA.
7. Many loss- and gain-of-function mutants affect LR development, but few only affect
LR development and/or root branching in a specic manner.
8. Several alternative approaches have proven useful in dening novel factors and global
responses in LR and adventitious root development, namely microarray, proteomic,
and, notably, QTL analyses.
FUTURE ISSUES
1. One outstanding question is whether one distinct pathway controls the initiation and
maintenance of root meristems in all root types, i.e., are the same molecular pathways
at play in primary roots as well as lateral and adventitious roots? Are differences in
the pathways initiating distinct root types due to context-specic use of homologous
factors, or do they reect the existence of altogether alternative pathways for root
formation?
2. What is the level of conservation of molecular mechanisms involved in root formation
and RSA modulation across distantly related species?
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3. What are the mechanistic modes of action of some important Arabidopsis proteins of
unknown function involved in root branching, such as ALF4 or BRX? Is their function
conserved in other plant species? Conversely, several novel genes important for RSA
have been discovered in model systems other than Arabidopsis. What are the specic
roles of genes like tomato DGT1 or rice LOB domain transcription factors in RSA,
and do they function in the same way in Arabidopsis?
4. One challenge facing those working in the rhizosphere is the inherent plasticity of
the root system. This challenge is mostly tackled by investigating root systems in
standardized tissue culture conditions. Is RSA modulation observed in tissue culture
really relevant for root systems in their native soil environment? Applying novel
imaging techniques for root systems grown in soil (e.g., X-ray imaging, computer
tomography) might help to address this question.
5. Analysis of natural genetic variation can be expected to become an increasingly useful
tool to determine the molecular genetic basis of RSA modulation.
6. Variation of RSA between and within species is commonly observed. Is this variation functionally signicant in an ecological context? For instance, do intraspecic
variations in RSA confer competitive advantages in particular conditions?
7. Model systems such as rice, maize, and poplar are becoming more tractable systems for
studying root development because of increasing availability of genetic and genomic
tools. To understand fully the conserved underlying mechanisms of root growth,
simple vascular plants (for example, ferns) should also be investigated in detail at the
molecular genetic level.
8. During the plant life cycle, the geotropism of roots changes. For instance, LRs emerge
from the parent root at a specic angle, but become geotropic after being diageotropic
or ageotropic for a long period of time. What molecular factors determine their
orientation and changes thereof with respect to the gravity vector?
ACKNOWLEDGMENTS
We apologize to those authors whose work could not be discussed owing to space restrictions.
Work in our lab is supported by the Swiss National Science Foundation and the Canton de
Vaud.
LITERATURE CITED
1. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, et al. 2004. The PLETHORA genes
mediate patterning of the Arabidopsis root stem cell niche. Cell 119:10920
2. Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, Nacry P, et al. 2003. Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signaling. Plant Cell Environ. 26:105366
3. Aloni R, Aloni E, Langhans M, Ullrich CI. 2006. Role of cytokinin and auxin in shaping
root architecture: regulating vascular differentiation, lateral root initiation, root apical
dominance and root gravitropism. Ann. Bot. 97:88393
4. Alonso-Blanco C, Koornneef M. 2000. Naturally occurring variation in Arabidopsis: an
underexploited resource for plant genetics. Trends Plant Sci. 5:2229
www.annualreviews.org Root System Architecture and Development
107
ANRV310-PP58-05
ARI
21 March 2007
19:14
5. Bao F, Shen J, Brady SR, Muday GK, Asami T, Yang Z. 2004. Brassinosteroids interact
with auxin to promote lateral root development in Arabidopsis. Plant Physiol. 134:162431
6. Bari R, Pant BD, Stitt M, Scheible WR. 2006. PHO2, microRNA399, and PHR1 dene
a phosphate-signaling pathway in plants. Plant Physiol. 141:98899
7. Beaudoin N, Serizet C, Gosti F, Giraudat J. 2000. Interactions between abscisic acid and
ethylene signaling cascades. Plant Cell 12:110315
8. Beeckman T, Burssens S, Inze D. 2001. The peri-cell-cycle in Arabidopsis. J. Exp. Bot.
52:40311
9. Benfey PN. 2005. Developmental networks. Plant Physiol. 138:54849
10. Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, et al. 1995. Superroot, a
recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:140519
11. Brady SM, Sarkar SF, Bonetta D, McCourt P. 2003. The ABSCISIC ACID INSENSITIVE
3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral
root development in Arabidopsis. Plant J. 34:6775
12. Brundrett MC. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytol.
154:275304
13. Casamitjana-Martinez E, Hofhuis HF, Xu J, Liu CM, Heidstra R, Scheres B. 2003. Rootspecic CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway
in the control of Arabidopsis root meristem maintenance. Curr. Biol. 13:143541
14. Casero PJ, Casimiro I, Lloret PG. 1995. Lateral root initiation by asymmetrical transverse
divisions of pericycle cells in 4 plant-species Raphanus sativus, Helianthus annuus, Zea
mays, and Daucus carota. Protoplasma 188:4958
15. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang HM, et al. 2003. Dissecting
Arabidopsis lateral root development. Trends Plant Sci. 8:16571
16. Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, et al. 2001. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:84352
17. Celenza JL J, Grisa PL, Fink GR. 1995. A pathway for lateral root formation in
Arabidopsis thaliana. Genes Dev. 9:213142
18. Chen CW, Yang YW, Lur HS, Tsai YG, Chang MC. 2006. A novel function of abscisic
acid in the regulation of rice (Oryza sativa L.) root growth and development. Plant Cell
Physiol. 47:113
19. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL. 2006. Regulation of phosphate
homeostasis by MicroRNA in Arabidopsis. Plant Cell 18:41221
20. Cluis CP, Mouchel CF, Hardtke CS. 2004. The Arabidopsis transcription factor HY5
integrates light and hormone signaling pathways. Plant J. 38:33247
21. Coates JC, Laplaze L, Haseloff J. 2006. Armadillo-related proteins promote lateral root
development in Arabidopsis. Proc. Natl. Acad. Sci. USA 103:162126
22. Correa-Aragunde N, Graziano M, Lamattina L. 2004. Nitric oxide plays a central role
in determining lateral root development in tomato. Planta 218:9005
23. Deak KI, Malamy J. 2005. Osmotic regulation of root system architecture. Plant J. 43:17
28
24. de Billy F, Grosjean C, May S, Bennett M, Cullimore JV. 2001. Expression studies on
AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early
nodule development. Mol. Plant Microbe. Interact. 14:26777
25. De Smet I, Signora L, Beeckman T, Inze D, Foyer CH, Zhang HM. 2003. An abscisic
acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J. 33:54355
26. De Smet I, Vanneste S, Inze D, Beeckman T. 2006. Lateral root initiation or the birth of
a new meristem. Plant Mol. Biol. 60:87187
108
Osmont
Sibout
Hardtke
ANRV310-PP58-05
ARI
21 March 2007
19:14
27. De Veylder L, de Almeida Engler J, Burssens S, Manevski A, Lescure B, et al. 1999. A new
D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation.
Planta 208:45362
28. Dharmasiri S, Swarup R, Mockaitis K, Dharmasiri N, Singh SK, et al. 2006. AXR4 is
required for localization of the auxin inux facilitator AUX1. Science 312:121820
29. DiDonato RJ, Arbuckle E, Buker S, Sheets J, Tobar J, et al. 2004. Arabidopsis ALF4 encodes
a nuclear-localized protein required for lateral root formation. Plant J. 37:34053
30. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, et al. 1993. Cellular organisation of the Arabidopsis thaliana root. Development 119:7184
31. Dong L, Wang L, Zhang Y, Deng X, Xue Y. 2006. An auxin-inducible F-box protein
CEGENDUO negatively regulates auxin-mediated lateral root formation in Arabidopsis.
Plant Mol. Biol. 60:599615
32. Drew MC. 1975. Comparison of effects of a localized supply of phosphate, nitrate, ammonium and potassium on growth of seminal root system, and shoot, in barley. New
Phytol. 75:47990
33. Esau K. 1965. Plant Anatomy. New York: Wiley
34. Feix G, Hochholdinger F, Park WJ. 2002. Maize root system and genetic analysis of its
formation. In Plant Roots: The Hidden Half, ed. Y Waisel, A Eshel, U Kafka, pp. 23948.
New York: Marcel Dekker
35. Feldman LJ. 1994. The maize root. In The Maize Handbook, ed. M Freeling, V Walbot,
pp. 2937. New York/Berlin: Springer-Verlag
36. Fiers M, Hause G, Boutilier K, Casamitjana-Martinez E, Weijers D, et al. 2004. Misexpression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of
root meristem. Gene 327:3749
37. Fitter AH. 1987. An architectural approach to the comparative ecology of plant-poot
systems. New Phytol. 106:6177
38. Fitz Gerald JN, Lehti-Shiu MD, Ingram PA, Deak KI, Biesiada T, Malamy JE. 2006.
Identication of quantitative trait loci that regulate Arabidopsis root system size and plasticity. Genetics 172:48598
39. Fu X, Harberd NP. 2003. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:74043
40. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK. 2005. A miRNA involved in phosphatestarvation response in Arabidopsis. Curr. Biol. 15:203843
41. Fukaki H, Tameda S, Masuda H, Tasaka M. 2002. Lateral root formation is blocked by a
gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J.
29:15368
42. Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, et al. 2002. The
regulation of nitrate and ammonium transport systems in plants. J. Exp. Bot. 53:85564
43. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S. 2002. Microarray analysis of
brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 130:131934
44. Hardtke CS. 2006. Root developmentbranching into novel spheres. Curr. Opin. Plant
Biol. 9:6671
45. Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, et al. 2004.
Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development
131:10891100
46. Harrison MJ. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annu. Rev.
Microbiol. 59:1942
www.annualreviews.org Root System Architecture and Development
109
ANRV310-PP58-05
ARI
21 March 2007
19:14
47. Hetrick BAD. 1991. Mycorrhizas and root architecture. Experientia 47:35562
48. Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inze D, Beeckman T.
2002. Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell
14:233951
49. Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, et al. 2004. Transcript
proling of early lateral root initiation. Proc. Natl. Acad. Sci. USA 101:514651
50. Hirsch AM, Lum MR, Downie JA. 2001. What makes the rhizobia-legume symbiosis so
special? Plant Physiol. 127:148492
51. Hobbie L, Estelle M. 1995. The axr4 auxin-resistant mutants of Arabidopsis thaliana dene
a gene important for root gravitropism and lateral root initiation. Plant J. 7:21120
52. Hobe M, Muller R, Grunewald M, Brand U, Simon R. 2003. Loss of CLE40, a protein
functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in
Arabidopsis. Dev. Genes Evol. 213:37181
53. Hochholdinger F, Park WJ, Sauer M, Woll K. 2004. From weeds to crops: genetic analysis
of root development in cereals. Trends Plant Sci. 9:4248
54. Horii H, Nemoto K, Miyamoto N, Harada J. 2005. Quantitative trait loci for adventitious
and lateral roots in rice. Plant Breed. 125:198200
55. Hou GC, Hill JP, Blancaor EB. 2004. Developmental anatomy and auxin response of
lateral root formation in Ceratopteris richardii. J. Exp. Bot. 55:68593
56. Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, et al. 2005. Crown rootless1,
which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE
FACTOR in auxin signaling. Plant Cell 17:138796
57. Ivanchenko MG, Coffeen WC, Lomax TL, Dubrovsky JG. 2006. Mutations in the
Diageotropica (Dgt) gene uncouple patterned cell division during lateral root initiation
from proliferative cell division in the pericycle. Plant J. 46:43647
58. Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, et al. 2003. Where do
gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J. 35:10415
59. Kim HB, Kwon M, Ryu H, Fujioka S, Takatsuto S, et al. 2006. The regulation of DWARF4
expression is likely a critical mechanism in maintaining the homeostasis of bioactive
brassinosteroids in Arabidopsis thaliana. Plant Physiol. 140:54857
60. King JJ, Stimart DP, Fisher RH, Bleecker AB. 1995. A mutation altering auxin homeostasis and plant morphology in Arabidopsis. Plant Cell 7:202337
61. Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, et al. 2006. An SNP caused loss of seed
shattering during rice domestication. Science 312:139296
62. Kutz A, Muller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW. 2002. A role for
nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana.
Plant J. 30:95106
63. Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R. 2006. Expression proling of
auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence.
Plant Cell Physiol. 47:78892
64. Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM. 1995. Formation of lateral root
meristems is a two-stage process. Development 121:330310
65. Leyser O. 2006. Dynamic integration of auxin transport and signaling. Curr. Biol.
16:R42433
66. Li J, Zhu SH, Song XW, Shen Y, Chen HM, et al. 2006. A rice glutamate receptor-like
gene is critical for the division and survival of individual cells in the root apical meristem.
Plant Cell 18:34049
110
Osmont
Sibout
Hardtke
ANRV310-PP58-05
ARI
21 March 2007
19:14
67. Linkohr BI, Williamson LC, Fitter AH, Leyser HM. 2002. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis.
Plant J. 29:75160
68. Little DY, Rao H, Oliva S, Daniel-Vedele F, Krapp A, Malamy JE. 2005. The putative
high-afnity nitrate transporter NRT2.1 represses lateral root initiation in response to
nutritional cues. Proc. Natl. Acad. Sci. USA 102:1369398
69. Liu HJ, Wang SF, Yu XB, Yu J, He XW, et al. 2005. ARL1, a LOB-domain protein
required for adventitious root formation in rice. Plant J. 43:4756
70. Liu Y, Lamkemeyer T, Jakob A, Mi GH, Zhang FS, et al. 2006. Comparative proteome
analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1. Proteomics 6:43008
71. Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM. 2004. Cytokinins play
opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J.
38:20314
72. Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L. 2003. The role of nutrient availability in regulating root architecture. Curr. Opin. Plant Biol. 6:28087
73. Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson
J, Herrera-Estrella L. 2002. Phosphate availability alters architecture and causes changes
in hormone sensitivity in the Arabidopsis root system. Plant Physiol. 129:24456
74. Lorbiecke R, Sauter M. 1999. Adventitious root growth and cell-cycle induction in deepwater rice. Plant Physiol. 119:2129
75. Loudet O, Gaudon V, Trubuil A, Daniel-Vedele F. 2005. Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana conrmed by heterogeneous
inbred family. Theor. Appl. Genet. 110:74253
76. Lynch J. 1995. Root architecture and plant productivity. Plant Physiol. 109:713
77. Malamy JE. 2005. Intrinsic and environmental response pathways that regulate root
system architecture. Plant Cell Environ. 28:6777
78. Malamy JE, Benfey PN. 1997. Organization and cell differentiation in lateral roots of
Arabidopsis thaliana. Development 124:3344
79. Malamy JE, Ryan KS. 2001. Environmental regulation of lateral root initiation in
Arabidopsis. Plant Physiol. 127:899909
80. McCully ME. 1999. Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:695718
81. Montiel G, Gantet P, Jay-Allemand C, Breton C. 2004. Transcription factor networks.
Pathways to the knowledge of root development. Plant Physiol. 136:347885
82. Moog PR, van der Kooij TA, Bruggemann W, Schiefelbein JW, Kuiper PJ. 1995. Responses to iron deciency in Arabidopsis thaliana: the Turbo iron reductase does not depend
on the formation of root hairs and transfer cells. Planta 195:50513
83. Mori M, Nomura T, Ooka H, Ishizaka M, Yokota T, et al. 2002. Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol.
130:115261
84. Mouchel CF, Briggs GC, Hardtke CS. 2004. Natural genetic variation in Arabidopsis
identies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the
root. Genes Dev. 18:70014
85. Mouchel CF, Osmont KS, Hardtke CS. 2006. BRX-mediated feedback between brassinosteroid levels and auxin signaling in root growth. Nature. 443:45861
86. Mussig C, Fischer S, Altmann T. 2002. Brassinosteroid-regulated gene expression. Plant
Physiol. 129:124151
www.annualreviews.org Root System Architecture and Development
111
ANRV310-PP58-05
ARI
21 March 2007
19:14
87. Mussig C, Shin GH, Altmann T. 2003. Brassinosteroids promote root growth in
Arabidopsis. Plant Physiol. 133:126171
88. Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, et al. 2005. A role for auxin
redistribution in the responses of the root system architecture to phosphate starvation in
Arabidopsis. Plant Physiol. 138:206174
89. Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, et al. 2003. Brassinolide induces
IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross
talk point of brassinosteroid and auxin signaling. Plant Physiol. 133:184353
90. Nemhauser JL, Mockler TC, Chory J. 2004. Interdependency of brassinosteroid and
auxin signaling in Arabidopsis. PLoS Biol. 2:E258
91. Olmos E, Kiddle G, Pellny T, Kumar S, Foyer C. 2006. Modulation of plant morphology,
root architecture, and cell structure by low vitamin C in Arabidopsis thaliana. J. Exp. Bot.
57:164555
92. Paszkowski U, Kroken S, Roux C, Briggs SP. 2002. Rice phosphate transporters include an
evolutionarily divergent gene specically activated in arbuscular mycorrhizal symbiosis.
Proc. Natl. Acad. Sci. USA 99:1332429
93. Ponce G, Barlow PW, Feldman LJ, Cassab GI. 2005. Auxin and ethylene interactions
control mitotic activity of the quiescent center, root cap size, and pattern of cap cell
differentiation in maize. Plant Cell Environ. 28:71932
94. Price NS, Roncadori RW, Hussey RS. 1989. Cotton root-growth as inuenced by
phosphorus-nutrition and vesicular arbuscular mycorrhizas. New Phytol. 111:6166
95. Przemeck GK, Mattsson J, Hardtke CS, Sung ZR, Berleth T. 1996. Studies on the role of
the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization.
Planta 200:22937
96. Remans T, Nacry P, Pervent M, Girin T, Tillard P, et al. 2006. A central role for the
nitrate transporter NRT2.1 in the integrated morphological and physiological responses
of the root system to nitrogen limitation in Arabidopsis. Plant Physiol. 140:90921
97. Rieer M, Novak O, Strnad M, Schmulling T. 2006. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:4054
98. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, et al. 2001. A conserved MYB
transcription factor involved in phosphate starvation signaling both in vascular plants
and in unicellular algae. Genes Dev. 15:212233
99. Salvi S, Tuberosa R. 2005. To clone or not to clone plant QTLs: present and future
challenges. Trends Plant Sci. 10:297304
100. Sauer M, Jakob A, Nordheim A, Hochholdinger F. 2006. Proteomic analysis of shootborne root initiation in maize (Zea mays L.). Proteomics 6:253041
101. Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, et al. 1994. Embryonic
origin of the Arabidopsis primary root and root meristem initials. Development 120:247587
102. Schiefelbein J. 2003. Cell-fate specication in the epidermis: a common patterning mechanism in the root and shoot. Curr. Opin. Plant Biol. 6:7478
103. Sergeeva LI, Keurentjes JJ, Bentsink L, Vonk J, van der Plas LH, et al. 2006. Vacuolar
invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant
analysis. Proc. Natl. Acad. Sci. USA 103:299499
104. Signora L, De Smet I, Foyer CH, Zhang HM. 2001. ABA plays a central role in mediating
the regulatory effects of nitrate on root branching in Arabidopsis. Plant J. 28:65562
105. Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, et al. 2005. Auxin and light control
of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17:134359
112
Osmont
Sibout
Hardtke
ANRV310-PP58-05
ARI
21 March 2007
19:14
106. Steffens B, Wang JX, Sauter M. 2006. Interactions between ethylene, gibberellin and
abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice.
Planta 223:60412
107. Steindler C, Matteucci A, Sessa G, Weimar T, Ohgishi M, et al. 1999. Shade avoidance
responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene
expression. Development 126:423545
108. Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM. 2005. A link between ethylene and
auxin uncovered by the characterization of two root-specic ethylene-insensitive mutants
in Arabidopsis. Plant Cell 17:223042
109. Swarup R, Parry G, Graham N, Allen T, Bennett M. 2002. Auxin cross-talk: integration
of signaling pathways to control plant development. Plant Mol. Biol. 49:41126
110. Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, et al. 2004. MASSUGU2
encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl
and formation of lateral roots in Arabidopsis thaliana. Plant Cell 16:37993
111. van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B. 1997. Short-range
control of cell differentiation in the Arabidopsis root meristem. Nature 390:28789
112. Wagner S, Bernhardt A, Leuendorf JE, Drewke C, Lytovchenko A, et al. 2006. Analysis
of the Arabidopsis rsr41/pdx13 mutant reveals the critical function of the PDX1 protein
family in metabolism, development, and vitamin B6 biosynthesis. Plant Cell 18:172235
113. Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG. 2006. Nitrogen regulation of root branching. Ann. Bot. 97:87581
114. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T. 2003.
Cytokinin-decient transgenic Arabidopsis plants show multiple developmental alterations
indicating opposite functions of cytokinins in the regulation of shoot and root meristem
activity. Plant Cell 15:253250
115. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM. 2001. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol. 126:87582
116. Woll K, Borsuk LA, Stransky H, Nettleton D, Schnable PS, Hochholdinger F. 2005.
Isolation, characterization, and pericycle-specic transcriptome analyses of the novel
maize lateral and seminal root initiation mutant rum1. Plant Physiol. 139:125567
117. Yokota T, Sato T, Takeuchi Y, Nomura T, Uno K, et al. 2001. Roots and shoots of
tomato produce 6-deoxo-28-norcathasterone, 6-deoxo-28-nortyphasterol and 6-deoxo28-norcastasterone, possible precursors of 28-norcastasterone. Phytochemistry 58:23338
118. Zhang H, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced
changes in root architecture. Science 279:4079
119. Zhang H, Jennings A, Barlow PW, Forde BG. 1999. Dual pathways for regulation of
root branching by nitrate. Proc. Natl. Acad. Sci. USA 96:652934
120. Zolobowska L, Van Gijsegem F. 2006. Induction of lateral root structure formation on
petunia roots: A novel effect of GMI1000 Ralstonia solanacearum infection impaired in
Hrp mutants. Mol. Plant-Microbe Interact. 19:597606
113