Genetics of Root Hair Formation
C. Grierson and J. Schiefelbein (*
ü)
Abstract There has been a great deal of recent progress in our understanding of the
genetic control of root hair development, particularly in Arabidopsis thaliana. This
chapter summarizes the genes and gene products that have been identified using forward
and reverse genetic approaches. The involvement of these genes at various stages of root
hair development is described, including the specification of the root hair cell type, the
initiation of the root hair outgrowth, and the elongation (tip growth) of the root hair.
1
Introduction
The formation of root hairs has been used for more than a century to study fundamental problems in plant biology, using physiological, cell biological, and developmental approaches (Cormack 1935; Cutter 1978; Haberlandt 1887; Leavitt 1904;
Sinnot and Bloch 1939). In the past 20 years, a great deal of attention has been
devoted to using genetics to study root hair formation, particularly in the model
plant species Arabidopsis. Arabidopsis root hairs are amenable to genetic dissection because (1) they are easily visible on the root surface and appear rapidly
(within 3 days) after seed germination, making them one of the most convenient
postembryonic cells for phenotypic analysis; (2) the entire developmental history
of the Arabidopsis epidermis has been defined, from its embryonic origin through
its mature cell features (Dolan et al. 1993, 1994; Scheres et al. 1994); (3) the root
epidermal cells are generated and differentiate in a file-specific manner, which
enables all stages of development to be analyzed along the root at any time; (4) the
root hair cells are not required for plant viability or fertility, and so any type of
mutant can be isolated and analyzed; (5) large-scale genetic screens are feasible,
since large numbers of seedlings can be analyzed for their root hair phenotype; and
J. Schiefelbein
Department of Molecular, Cellular, and Developmental Biology,
University of Michigan, 830 North University Avenue, Natural Sciences Building,
Ann Arbor MI 48109-1048, USA
e-mail: [email protected]
Plant Cell Monogr, doi:10.1007/7089_2008_15
© Springer-Verlag Berlin Heidelberg 2008
1
2
C. Grierson, J. Schiefelbein
(6) molecular and genomic resources are available in Arabidopsis for the rapid
analysis of new genes and proteins.
In this chapter, we describe the genetics of root hair cell specification, root hair
initiation, and root hair growth (elongation). A list of the genes identified from
Arabidopsis is presented in Table 1.
Table 1 Genes involved in root hair formation in Arabidopsis
Genea
Root hair mutant
phenotype
Arabinogalactan
protein
Short root hairs
Actin-interacting
AIP1
protein
Long root hairs
Potassium transAKT1
porter
None
Rab GTPase
ARA6
Dominant mutants have no ADP-ribosylation
ARF1
hairs, or have short or
factor GTPases
double root hairs
Reduced root hair length Exocyst subunit
AtEXO70A1
Exo70
Long root hairs
Inositol polyphosAtIPK2α
phate kinase
Short hairs
Auxin transport
AUX1
Bulges form but do not
Subunit of RUB1AXR1
elongate
activating
enzyme
Dominant mutants are
Repressor of auxinAXR2/IAA7
hairless, except where
responsive tranroot meets hypocotyl
scription
Dominant mutants are
Repressor of
AXR3/IAA17
hairless, except where
auxin-responsive
root meets hypocotyl
transcription
High phosphate does not bHLH transcription
BHLH32
suppress root hair
factor
development
Short hairs in high phos- Calossin
BIG
phate conditions
Short hairs, sometimes
Unknown
BRISTLED1
branched
(BST1)/DER4
Hairs short, bulbous, occa- Actin-binding proCAP1
sionally branched
tein
Vegetative actin
CEN3/DER1/ACT2 Short, wide hairs, some
with wide bases, some
hairs curled and/or
branched
Short, wide hairs, someUnknown
CENTIPEDE1
times curled
(CEN1)
Short, wide hairs, someUnknown
CENTIPEDE2
times branched and/or
(CEN2)
curled
AGP30
None
Predicted product
Reference
van Hengel et al. 2004
Ketelaar et al. 2007
Desbrosses et al. 2003
Grebe et al. 2003
Xu and Scheres 2005
Synek et al. 2006
Xu et al. 2005b
Pitts et al. 1998
Cernac et al. 1997; del
Pozo et al. 2002
Nagpal et al. 2000
Leyser et al. 1996
Chen et al. 2007
Lopez-Bucio et al. 2005
Parker et al. 2000;
Ringli et al. 2005
Deeks et al. 2007
Ringli et al. 2002
Parker et al. 2000
Parker et al. 2000
(continued)
Genetics of Root Hair Formation
3
Table 1 (continued)
Genea
COW1
CPC
DER2
DER3/ENL7
DER5
DER6
DER7
DER8
EGL3
EIN2
ENL1
ENL5
EPC1
ETC1
ETO1-4
ETR1, ERS1,
ERS2, ETR2
EXP18
EXP7
GL2
GL3
IAA14
ICR1
IRE
KEULE
Root hair mutant
phenotype
Predicted product
Reference
Short, wide root hairs,
Phosphatidylinositol Bohme et al. 2004;
often branched at the
transfer protein
Vincent et al. 2005
base
Reduced root hair number R3 Myb transcripWada et al. 2002
tion factor
Hairs stop growing after
Unknown
Ringli et al. 2005
bulge forms
Hairs have wide bases and Unknown
Ringli et al. 2005
sometimes branch
Short, distorted hairs
Unknown
Ringli et al. 2005
Very short hairs
Unknown
Ringli et al. 2005
Hairs often short, wide,
Unknown
Ringli et al. 2005
and bulbous
Hairs often depolarized
Unknown
Ringli et al. 2005
None
bHLH transcription Bernhardt et al. 2005
factor
Root hairs form further
Ethylene response
Fischer et al. 2006
from the end of the
epidermal cell
Wavy, branched hairs
Unknown
Diet et al. 2004
Short, wide, curved hairs Unknown
Diet et al. 2004
Short root hairs
Glycosyltransferase Bown et al. 2007
None
R3 Myb transcripKirik et al. 2004a
tion factor
Cao et al. 1999
Increased root hair length Ethylene overproand density
ducer
Reduced root hair length Ethylene receptor
Cho and Cosgrove 2002
–
None
Excess root hairs
Expansin protein
Expansin protein
Homeodomain-leucine-zipper transcription factor
Increased root hair number bHLH transcription
factor
Dominant mutants are
Repressor of auxinhairless, except where
responsive tranroot meets hypocotyl
scription
In loss-of-function mutant Coiled-coil domain
hairs form closer to
scaffold protein
the root tip. Ectopic
regulated by
expression produces
ROPs
short, bulbous root
hairs
Short root hairs
Serine/threonine
kinase
Hairs absent or stunted
Sec1 protein
and swollen
Cho and Cosgrove 2002
Cho and Cosgrove 2002
Masucci et al. 1996
Bernhardt et al. 2005
Fukaki et al. 2002
Lavy et al. 2007
Oyama et al. 2002
Assaad et al. 2001
(continued)
4
C. Grierson, J. Schiefelbein
Table 1 (continued)
Genea
Root hair mutant
phenotype
KIP
KJK/SHV1/
AtCSLD3
Wide hairs
Hairs burst after bulge
forms
LPI1
MRH1
Root hair length and density less affected by
high phosphate
Root hair length less
affected by high phosphate
Hairs short, swollen, or
branched
Some hairs short, swollen,
or branched
Short hairs
MRH2
Wavy, branched hairs
MRH3
Hairs have wide bases
Myosin XIK
Hairs short and slowgrowing
Variable root hair length
LPI2
LRX1
LRX2
OXI1/AGC2
PLDζ1
PRP3
Suppressor of dominant
mutations in AXR3,
pax1 single mutant has
extra root hairs that are
sometimes branched
Overexpressing root hairs
twice as long as wild
type
Long hairs
Double mutant with PI4Kβ2 has branched,
wavy and bulged root
hairs
Short, wide hairs.
Overexpressors have
fat, curled or bulbous
hairs
None
None
RABA4b
None
PAX1
PFN1
PGP4
PI-4Kß1
PIP5K3
Predicted product
Reference
SABRE-like protein Procissi et al. 2003
ER-localized cell
Favery et al. 2001
wall polysaccharide synthase
Unknown
Sanchez-Calderon et al.
2006
Unknown
Sanchez-Calderon et al.
2006
Leucine-rich repeat
(LRR)/extensin
LRR/extensin
Baumberger et al. 2001
LRR class of receptor-like kinase
Armadillo repeat
containing
kinesin-related
protein
Inositol 1,4,5-triphosphate 5phosphatase
Myosin XI
Jones et al. 2006
Ojangu et al. 2007
Oxidative-burstinducible kinase
Unknown
Anthony et al. 2004;
Rentel et al. 2004
Tanimoto et al. 2007
Profilin
Ramachandran et al.
2000
Baumberger et al. 2003
Jones et al. 2006
Jones et al. 2006
Auxin transport
Santelia et al. 2005
Phosphatidylinositol Preuss et al. 2006
4-OH kinase
Phosphatidylinositol- Stenzel et al. 2008
4-phosphate 5kinase
Phospholipase D
Ohashi et al. 2003
Proline-rich cell wall Bernhardt and Tierney
protein
2000
Rab GTPase
Preuss et al. 2004
(continued)
Genetics of Root Hair Formation
5
Table 1 (continued)
Genea
Root hair mutant
phenotype
RHD1/UGE4
RHD2
RHD3
RHD6
RHL1, RHL2,
RHL3
RHM1/ROL1
RPA/At2G35210
SAR1
SCN1
SHV2/COBL9/
DER9/MRH4
SHV3/MRH5
SIMK
SIZ1
SOS4
TIP1
TRH1
TRY
TTG
WER
WRKY75
a
Predicted product
Reference
Wide swellings
UDP-d-glucose 4epimerase
Hairs stop growing after
bulge forms
Wavy, short hairs
NADPH oxidase
Schiefelbein and
Somerville 1990;
Seifert et al. 2002
Foreman et al. 2003
GTP-binding protein
involved in ER–
Golgi transport
Hairless
Unknown
Reduced root hair density, Topoisomerase
dwarf
subunits
Suppressor of lrx1
Pectic polysaccharide rhamnogalacturonan
modifying
enzyme
Short, bulbous and
ARF GTPase-actibranched root hairs
vating protein
Suppressor of axr1
Nucleoporin
Short, wide, hairs, some- ROPGDP dissociatimes branched
tion inhibitor
Hairs stop growing after
COBRA-like protein
bulge forms
Hairs stop growing after
Glycerophosphoryl
bulge forms
diester phosphodiesterase
(GPDP)-like
protein
Overexpression increases Mitogen-activated
protein kinase
root hair length
Long root hairs very near SUMO E3 ligase
root tip
Bulges form but do not
Pyridoxal kinase
elongate
Wide swellings; short,
ANK protein S-acyl
wide hairs, branched
transferase
at base
Hairs stop growing after
Potassium carrier
bulge forms. Some
required for
cells with multiple
auxin transport
bulges
None
R3 Myb transcription factor
Excess root hairs
WD-repeat protein
Excess root hairs
R2R3 Myb transcription factor
Increased root hair density Transcriptional
repressor
Wang et al. 1997; Zheng
et al. 2004
Menand et al. 2007
Sugimoto-Shirasu et al.
2002, 2005
Diet et al. 2006
Song et al. 2006
Cernac et al. 1997
Carol et al. 2005
Jones et al. 2006
Jones et al. 2006
Samaj et al. 2002
Miura et al. 2005
Shi and Zhu 2002
Hemsley et al. 2005
Rigas et al. 2001
Schellmann et al. 2002
Galway et al. 1994
Lee and Schiefelbein
1999
Devaiah et al. 2007
Multiple names for the same gene are given when these are used in the literature