with the environment is fundamental to the biology of all organisms, and
especially to plants. Our research group investigates key aspects of this
relationship, focusing on the ways in which environment changes plant biology
over a wide range of timescales: from the short-term physiological adaptation
of individual plants to fluctuating environments, to the long-term effects of environment
on plant evolution. Our approaches are unified by the use of genetics, with a
strong emphasis on whole-genome sequencing, and we work with a variety of model
and crop plant systems (Arabidopsis thaliana, Physcomitrella patens,
wheat) appropriate to particular research questions. Our coordinated interests cover
both fundamental questions (e.g., How does mutation contribute to plant
evolution?) and practical outcomes (e.g., Can we improve the salt-tolerance of
crop plants?). Specific interests are outlined below (see Current Projects).
August 2007) our research group was located at the John Innes Centre, Norwich,
and focused on the genetics of plant growth regulation by the phytohormone
gibberellin. We revealed the nature and biological properties of the
gibberellin-DELLA mechanism (the mechanism via which gibberellin promotes plant
growth), and showed that a variant form of this mechanism causes the dwarfism
characteristic of the high-yielding wheat varieties of the 'green revolution'.
We also showed that the gibberellin-DELLA mechanism integrates the effects of
multiple environmental signals, and that it provides plants with the capacity
to regulate their growth in response to environmental change. We also
determined how the gibberellin-DELLA mechanism evolved during land-plant
evolution, showing how the modern angiosperm mechanism was derived by a series
of steps from precursor components present in the earliest diverging
contacts from prospective graduate students and postdoctoral researchers.
currently four interrelated areas of research in the lab:
interested in the role that de novo DNA sequence mutation plays in
evolution, and in determining the extent to which the environment influences
this process. This project involves whole-genome studies of A. thaliana. We
initially developed (in collaboration with Prof. Richard Mott at the University
of Oxford Wellcome Trust Centre for Human Genetics) robust methods for the
identification of de novo DNA sequence mutations in ‘short-read’ whole
genome DNA sequencing datasets. We are now amongst the world leaders in de
novo mutation detection, and are applying our methods to understand how de
novo mutations arise. For example, although it has long been known that
exposure to environmental fast-neutron (FN) irradiation is mutagenic, the
genome-wide effects of fast-neutron irradiation were poorly understood. We have
recently shown that, in contrast to what was previously thought, FN exposure
causes more base substitution mutations than deletion mutations, and that these
substitutions exhibit a characteristic molecular mutational spectrum (a
reflection of the different frequencies of specific transition and transversion
mutations) that is very different from that exhibited by mutations arising
spontaneously in control plants (Belfield et al., 2012).
In further recent
studies, we have investigated the fascinating phenomenon of plant somaclonal
variation. When whole plants are regenerated from cells grown in in vitro cell
culture conditions, these plants often exhibit high frequencies of heritable
phenotypic variation, a phenomenon known as somaclonal variation. Until
recently, the underlying causes of somaclonal variation were poorly understood.
We have advanced understanding of this phenomenon by showing that base
substitution mutation is a major cause of somaclonal variation, and that the
molecular mutational spectrum of mutations arising during plant regeneration is
again very different from that of mutations arising spontaneously in control
plants (Jiang et al., 2011).
we are extending our studies by experimental analysis of the effects of
environment on genome-wide inherited de novo mutations in plants, and
via comparison of resultant findings with the spectrum of SNP mutations found
in natural variant A. thaliana strains and base substitutions
distinguishing Arabidopsis species (Belfield et al., unpublished;
Jiang et al., unpublished; Gan et al., 2011).
to Environmental Stress: Salt-Stress
working on plant salt-stress responses as a fundamental model of how plants
respond physiologically to the challenge of stressful environments, and because
salt-stress is a major global threat to the yields of crop plants. Our work
involves investigations with A. thaliana and with wheat. Our A.
thaliana studies involve both induced mutational and natural variation
approaches to the study of the responses of plants to high-salinity soils. In
the mutational studies we have selected for mutants exhibiting either increased
resistance or increased sensitivity to growth on saline soils. These studies
have enabled substantial advance in understanding, because previous studies of A.
thaliana salt-stress responses have mostly been conducted in
low-transpiration petri-dish environments. In contrast, our studies more
closely reflect the reality of plants growing in the wild or in the field, in
which the transpiration stream is a major conduit of water and salts through
the xylem vasculature from the root to the shoot of plants. In collaboration
with Prof. Andrew Smith (University of Oxford Department of Plant Sciences) we
have shown that levels of reactive oxygen species (ROS) in the region of the
root vasculature regulate the sodium (Na) content of xylem sap, and that these
ROS levels are themselves controlled by Na sensitive regulation of the activity
of a specific respiratory burst oxidase enzyme (encoded by the gene AtrbohF)
catalyzing ROS production. Thus we have discovered a ROS-regulated mechanism
for regulation of root-to-shoot delivery of soil Na, a discovery that has major
implications both for our understanding of how plants maintain internal ionic
homeostasis, and for the hugely important goal of improving the
salinity-tolerance of diverse agricultural crops (Jiang et al.,
We are also
investigating the cause of natural variation in response to soil salinity using
a set of ‘MAGIC’ lines derived by intercrossing of 18 different founder A.
thaliana lines sourced from throughout the global distribution range of
this species. The aim of this project is to correlate phenotypic variation with
inheritance of specific founder alleles, thus identifying the genes that are
causal in determining the range of soil salinity tolerance in A. thaliana growing
in the wild. The identification of these genes will then enable targeting of
orthologous genes in crop species, with the eventual aim once again of developing
salinity-tolerant crop strains.
are also investigating the effects of salt-stress on the biology of wheat and
of related grass species (see below).
discoveries of previously unknown mechanisms via which plants achieve
physiological adaptation to a saline-soil environment have important practical
implications. Soil salinity is a major factor limiting agricultural production,
and affects an estimated ~20 million hectares of cultivated land world-wide. Furthermore,
the global area of salinized cultivated land is rapidly increasing due to the
widespread use of irrigation systems, thus threatening global food security. There
is therefore an urgent need to understand plant soil-salinity tolerance
mechanisms, and to identify genes conferring tolerance. Our elucidation of the
mechanisms of transpiration-dependent salt tolerance has particular relevance
to crops growing in field environments, and to the need to improve both
salinity tolerance and water-use efficiency in agriculture.
transcript balance, environmental effects and salt-tolerance
Wheat is a
crop-plant of major global food-security importance, and presents an exciting
scientific challenge due to the size and complexity of its genome. Our research
on wheat focuses on understanding the regulation of gene expression at a
genome-wide level, with special reference to the effects of the environment on
complexity of wheat is due in part to its being a polyploid genome comprising
three distinct A, B and D homoeologous subgenomes. In essence, many of the
individual genes in the wheat genome are represented by three different A, B
and D homeoalleles. Very little is known in a genome-wide sense of the relative
extents to which individual A, B and D homeoalleles contribute to the overall
expression of an individual gene. We are comparing genome-wide RNA-seq datasets
obtained from Chinese Spring (euploid) wheat and from nullisomic-tetrasomic
lines lacking individual wheat chromosomes to determine, on a gene-by-gene basis,
the relative transcript-level contributions of individual homeoalleles. Our
findings (Leach et al., unpublished) are of fundamental biological
interest, because they provide the beginnings of a systematic understanding of
how homoeologous gene expression is coordinately regulated in polyploids. In
addition, our findings have important implications for wheat breeders, because
they enable understanding of the relative extents to which individual
homeoalleles contribute to the traits that need to be improved to for
sustainable increases in yield.
experiments, we are determining the extent to which environment (salt-stress)
affects the relative expression levels of wheat homeoalleles, as a route to
understanding wheat salinity responses. Finally, in collaboration with Prof.
Ian King (University of Nottingham), we are taking an RNA-seq approach to
understanding the salt-tolerance conferred on wheat by the introduction of
chromosomes from the wild salt-tolerant wheat relative Thinopyrum
of Environmental Responses
has a long-term interest in understanding how plant growth-regulatory (Yasumura
et al., 2007) and environmental response mechanisms evolved. We are
currently investigating the evolution of ethylene-mediated regulation of plant
submergence responses (Yasumura et al., submitted).
Our work (1997-2012) has
been funded by the BBSRC, The Gatsby Charitable Foundation, the European Union
and the King Abdullah University of Science and Technology.
Yasumura, Y., Crumpton-Taylor, M., Fuentes, S. & Harberd, N. P.
acquisition of the gibberellin-DELLA growth-regulatory mechanism during
land-plant evolution. Current Biology 17, 1225-1230.
Achard, P., Baghour, M., Chapple, A., Hedden, P., Van Der Straeten, D.,
Genschik, P., Moritz, T. & Harberd, N. P. (2007). The plant stress hormone ethylene controls floral transition via
DELLA-dependent regulation of floral meristem-identity genes. Proceedings of
the National Academy of Sciences of the United States of America 104,
Jiang, C., Gao, X., Liao, L., Harberd, N.P. & Fu, X. (2007). Phosphate starvation root architecture and anthocyanin
accumulation responses are modulated by the gibberellin-DELLA signaling pathway
in Arabidopsis. Plant Physiology 145, 1460-1470.
Achard, P., Liao, L., Jiang, C., Desnos, T., Bartlett, J., Fu, X. & Harberd,
N. P. (2007). DELLAs contribute to
plant photomorphogenesis. Plant Physiology 143, 1163-1172.
Harberd, N. (2006). Seed to Seed:
the secret life of plants. Bloomsbury (UK/USA).
Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T.,
Van Der Straeten, D., Peng, J. & Harberd, N. P. (2006). Integration of plant responses to environmentally
activated phytohormonal signals. Science 311, 91-94.
Sablowski, R. & Harberd, N. P. (2005). Plant
genes on steroids. Science 307, 1569-1570.
Alvey, L. & Harberd, N. P. (2005). DELLA
proteins: integrators of multiple plant growth regulatory inputs? Physiologia
Plantarum 123, 153-160.
Vriezen, W. H., Achard, P., Harberd, N. P. & Van Der Straeten, D.
(2004).Ethylene-mediated enhancement of
apical hook formation in etiolated Arabidopsis thaliana seedlings is
gibberellin dependent. Plant Journal 37, 505-516.
Fu, X., Richards, D. E., Fleck, B., Xie, D., Burton, N. & Harberd, N. P.
(2004).The Arabidopsis mutant sleepy1gar2-1
protein promotes plant growth by increasing the affinity of the SCFSLY1 E3
ubiquitin ligase for DELLA protein substrates. Plant Cell 16, 1406-1418.
Cheng, H., Qin, L., Lee, S., Fu, X., Richards, D. E., Cao, D., Luo, D.,
Harberd, N. P. & Peng, J. (2004). Gibberellin
regulates Arabidopsis floral development via suppression of DELLA protein
function. Development 131, 1055-1064.
Achard, P., Herr, A., Baulcombe, D. C. & Harberd, N. P. (2004). Modulation of floral development by a
gibberellin-regulated microRNA. Development 131, 3357-3365.
Petty, L. M., Harberd, N. P., Carre, I. A., Thomas, B. & Jackson, S. D.
(2003).Expression of the Arabidopsis gai
gene under its own promoter causes a reduction in plant height in chrysanthemum
by attenuation of the gibberellin response. Plant Science 164, 175-182.
Hynes, L. W., Peng, J., Richards, D. E. & Harberd, N. P. (2003). Transgenic expression of the Arabidopsis DELLA
proteins GAI and gai confers altered gibberellin response in tobacco.
Transgenic Research 12, 707-714.
Harberd, N. P. (2003). Relieving DELLA
restraint. Science 299, 1853-1854.
Fu, X. & Harberd, N. P. (2003). Auxin
promotes Arabidopsis root growth by modulating gibberellin response. Nature
Ait-ali, T., Rands, C. & Harberd, N. P. (2003). Flexible control of plant architecture and yield via
switchable expression of Arabidopsis gai. Plant Biotechnology journal 1,
Achard, P., Vriezen, W. H., Van Der Straeten, D. & Harberd, N. P.
(2003).Ethylene regulates arabidopsis
development via the modulation of DELLA protein growth repressor function.
Plant Cell 15, 2816-2825.
Peng, J., Richards, D. E., Moritz, T., Ezura, H., Carol, P. & Harberd,
N. P. (2002). Molecular and
physiological characterization of Arabidopsis GAI alleles obtained in targeted
Ds-tagging experiments. Planta 214, 591-596.
Peng, J. & Harberd, N. P. (2002). The
role of GA-mediated signalling in the control of seed germination. Current
opinion in plant biology 5, 376-381.
Lee, S., Cheng, H., King, K. E., Wang, W., He, Y., Hussain, A., Lo, J.,
Harberd, N. P. & Peng, J. (2002). Gibberellin
regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose
expression is up-regulated following imbibition. Genes & Development 16,
Fu, X., Richards, D. E., Ait-Ali, T., Hynes, L. W., Ougham, H., Peng, J.
& Harberd, N. P. (2002).
Gibberellin-mediated proteasome-dependent degradation of the barley DELLA
protein SLN1 repressor. Plant Cell 14, 3191-3200.
Fleck, B. & Harberd, N. P. (2002). Evidence that the Arabidopsis nuclear gibberellin signalling protein GAI
is not destabilised by gibberellin. Plant Journal 32, 935-947.
Richards, D. E., King, K. E., Ait-Ali, T. & Harberd, N. P. (2001). How gibberellin regulates plant growth and
development: A Molecular Genetic Analysis of Gibberellin Signaling. Annual
Review of Plant Physiology and Plant Molecular Biology 52, 67-88.
King, K. E., Moritz, T. & Harberd, N. P. (2001). Gibberellins are not required for normal stem growth
in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159, 767-776.
Fu, X., Sudhakar, D., Peng, J., Richards, D. E., Christou, P. & Harberd,
N. P. (2001). Expression of Arabidopsis
GAI in transgenic rice represses multiple gibberellin responses. Plant Cell 13,
Desnos, T., Puente, P., Whitelam, G. C. & Harberd, N. P. (2001). FHY1: a phytochrome A-specific signal transducer.
Genes andDevelopment 15, 2980-2990.
Richards, D. E., Peng, J. & Harberd, N. P. (2000). Plant GRAS and metazoan STATs: one family? Bioessays
Collett, C. E., Harberd, N. P. & Leyser, O. (2000). Hormonal interactions in the control of
Arabidopsis hypocotyl elongation. Plant Physiology 124, 553-562.
Peng, J., Richards, D. E., Moritz, T., Cano-Delgado, A. & Harberd, N. P.
(1999a). Extragenic suppressors of the
Arabidopsis gai mutation alter the dose-response relationship of diverse
gibberellin responses. Plant Physiology 119, 1199-1208.
Peng, J., Richards, D. E., Hartley, N. M., Murphy, G. P., Devos, K. M.,
Flintham, J. E., Beales, J., Fish, L. J., Worland, A. J., Pelica, F., Sudhakar,
D., Christou, P., Snape, J. W., Gale, M. D. & Harberd, N. P. (1999b). 'Green revolution' genes encode mutant
gibberellin response modulators. Nature 400, 256-261.
Ezura H., Higashi, K. & Harberd, N. P. (1999). Phytochrome B influences in-vitro shoot morphogenesis
in Arabidopsis thaliana (L.) Heyhn. Plant Biotechnology 16, 279-284.
Cowling, R. J. & Harberd, N. P. (1999). Gibberellins control Arabidopsis hypocotyl growth via regulation of
cellular elongation. Journal of Experimental Botany 50, 1351-1357.
Harberd, N. P., King, K. E., Carol, P., Cowling, R. J., Peng, J. &
Richards, D. E. (1998). Gibberellin:
inhibitor of an inhibitor of...? Bioessays 20, 1001-1008.
Cowling, R. J., Kamiya, Y., Seto, H. & Harberd, N. P. (1998). Gibberellin dose-response regulation of GA4 gene
transcript levels in Arabidopsis. Plant Physiology 117, 1195-1203.
Peng, J. & Harberd, N. P. (1997). Transposon-associated
somatic gai-loss sectors in Arabidopsis. Plant Science 130, 181-188.
Peng, J. & Harberd, N. P. (1997). Gibberellin
deficiency and response mutations suppress the stem elongation phenotype of
phytochrome-deficient mutants of Arabidopsis. Plant Physiology 113, 1051-1058.
Peng, J., Carol, P., Richards, D. E., King, K. E., Cowling, R. J., Murphy,
G. P. & Harberd, N. P. (1997). The
Arabidopsis GAI gene defines a signaling pathway that negatively regulates
gibberellin responses. Genes and Development 11, 3194-3205.
Prof. David Baulcombe, University of Cambridge.
Prof. Dominique Van Der Straeten, Ghent, Belgium.
Prof. Ian King, University of Nottingham.
Dr. Ioannis Ragoussis, WTCHG, Oxford.
Prof. Jinrong Peng, ICMB, Singapore.
Prof. John Snape, JIC, Norwich.
Prof. Jonathan Jones, Sainsbury Lab, Norwich.
Dr. Margaret Boulton, JIC, Norwich.
Prof. Ottoline Leyser, Sainsbury Laboratory, Cambridge University.
Prof. Pascal Genschik, IBMP, Strasbourg, France.
Dr. Patrick Achard, IBMP, Strasbourg, France.
Prof. Richard Mott, WTCHG, Oxford.
Mr. Steve Reader, JIC, Norwich.
Dr. Thomas Moritz, Umeå, Sweden.
Dr. Toshi Foster, HortResearch, New Zealand.
Dr. Xiangdong Fu, Beijing, China.
Prof. Yuji Kamiya, RIKEN, Japan.