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Mutation, Evolution and Environmental Response
The relationship 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. We also have particular interests in how plants coordinate the regulation of their growth with their acquisition of carbon and mineral nutrient resources from the environment. These particular interests arise from our previous world-leading work on the gibberellin-DELLA mechanism and our discovery of the mechanisms via which ‘green revolution’ crop varieties are altered in this coordination (see below). Our approaches are unified by the use of genetics, with a strong emphasis on whole-genome sequencing, and we use both model and crop plant systems (Arabidopsis thaliana, rice and 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 nutrient use efficiency (NUE) or soil-salinity tolerance of crop plants?). Specific interests are outlined below (see Current Projects).
Previously (until 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 land-plants.
We welcome contacts from prospective graduate students and postdoctoral researchers.
There are currently three interrelated areas of research in the lab:
Mutation and Evolution
We are 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 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).
More recently, we have extended these studies by experimental analysis of the effects of environment on genome-wide inherited de novo mutations in plants. Our recent analysis of the effects of growing plants in stressful high-salinity soil environments has shown that the environment influences both rate and molecular spectrum of accumulated mutations, and also changes the patterns of inherited epigenetic changes in cytosine methylation status (Jiang et al., 2014).
Our studies in the area of Mutation and Evolution are unified by the concept that an understanding of the effects of the natural environment on the accumulation of mutations is necessary for a full understanding of how evolution works.
Towards Molecular Breeding of 21st Century ‘Super-Green Revolution’ Crop Varieties
Ensuring future global food security is a major humanitarian challenge. The needs of the around 9 billion people expected by 2050 require a two-fold increase in crop productivity. This increase must be achieved with minimal environmental damage. In the second half of the 20th century, the introduction of high-yielding cereal ‘Green Revolution’ Varieties (GReVs) began progressive crop productivity increases. However, these increases have recently plateaued. Furthermore, GReVs have low soil mineral nutrient use efficiency (NUE), and are dependent for high yield upon environmentally unsustainable fertilizer applications.
A new approach to yield breeding is essential: the molecular breeding of 21st century ‘Super-Green Revolution’ Crop Varieties (SuGReVs). We previously discovered the molecular identity of the Rht ‘green revolution’ gene variants of wheat GReVs, showing that variant forms of the gibberellin-DELLA mechanism are crucial to yield. These previous insights give us a unique vision for the development of SuGReVs. Our vision builds upon new understanding of the biology of GReVs, and of plant mineral nutrient uptake and assimilation. It exploits revolutionary ‘genome-editing’ technologies, and extant natural genetic variation.
We are currently seeking funding for this project. In summary, we will use state-of-the-art molecular breeding techniques to transform GReVs into SuGReVs. These SuGReVs will produce increased grain yields with reduced fertiliser input, thus promoting future global food security and reducing environmental damage.
Plant Responses to Environmental Stress: Salt-Stress
We are 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 in this area involves mutational investigations with A. thaliana, with a special focus on the responses of plants to high-salinity soils. We have selected 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., 2012; Jiang et al., 2013).
Our novel 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 ~62 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.
Publications (while at this department)
Belfield, E.J., Ding, Z.J., Jamieson, F.J.C., Visscher, A.M., Zheng, S.J., Mithani, A., Harberd, N.P. DNA mismatch repair preferentially protects genes from mutation (2018) Genome Research, 28 (1), pp. 66-74. DOI: 10.1101/gr.219303.116
Imprialou M, Kahles A, Steffen JG, Osborne EJ, Gan X, Lempe J, Bhomra A, Belfield E, Visscher A, Greenhalgh R, Harberd NP, Goram R, Hein J, Robert-Seilaniantz A, Jones J, Stegle O, Kover P, Tsiantis M, Nordborg M, Rätsch G, Clark RM, Mott R (2017). Genomic Rearrangements in Arabidopsis Considered as Quantitative Traits. Genetics. 205(4):1425-1441.
Zhang, M., Smith, J.A.C., Harberd, N.P., Jiang, C. The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses (2016) Plant Molecular Biology, 91 (6), pp. 651-659.
Khan, A., Belfield, E.J., Harberd, N.P., Mithani, A. HANDS2: Accurate assignment of homoeallelic base-identity in allopolyploids despite missing data (2016) Scientific Reports, 6, art. no. 29234, .
Liu, Q., Harberd, N.P., Fu, X. SQUAMOSA Promoter Binding Protein-like Transcription Factors: Targets for Improving Cereal Grain Yield (2016) Molecular Plant, 9 (6), pp. 765-767.
Chen, X., Yao, Q., Gao, X., Jiang, C., Harberd, N.P., Fu, X. Shoot-to-Root Mobile Transcription Factor HY5 Coordinates Plant Carbon and Nitrogen Acquisition (2016) Current Biology, 26 (5), pp. 640-646.
Harberd, N.P. Shaping Taste: The Molecular Discovery of Rice Genes Improving Grain Size, Shape and Quality (2015) Journal of Genetics and Genomics, 42 (11), pp. 597-599.
Visscher, A.M., Belfield, E.J., Vlad, D., Irani, N., Moore, I., Nicholas, Harberd, P. Overexpressing the multiple-stress responsive gene At1g74450 reduces plant height and male fertility in Arabidopsis thaliana (2015) PLoS ONE, 10 (10), art. no. e0140368,
Yasumura, Y., Pierik, R., Kelly, S., Sakuta, M., Voesenek, L.A.C.J., Harberd, N.P. An ancestral role for CONSTITUTIVE TRIPLE RESPONSE1 proteins in both ethylene and abscisic acid signaling (2015) Plant Physiology, 169 (1), pp. 283-298.
B2014) Microarray-based optimization to detect genomic deletion mutations Genomics Data. 2: pp 53-54.
2014) Microarray-based ultra-high resolution discovery of genomic deletion mutations BMC Genomics. 15 (1):.
2014) Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res.. 24 (11): pp 1821-1829.
2014) Patterns of homoeologous gene expression shown by RNA sequencing in hexaploid bread wheat BMC Genomics. 15 (1):.
2013) An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis Plant Cell. 25 (9): pp 3535-3552.
2013) HANDS: A tool for genome-wide discovery of subgenome-specific base-identity in polyploids BMC Genomics. 14 (1):.
2012) Genome-wide analysis of mutations in mutant lineages selected following fast-neutron irradiation mutagenesis of Arabidopsis thaliana Genome Research..
2012) Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses Plant Cell. 24 (10): pp 3982-3996.
2012) ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis EMBO Journal..
2012) Transcription factor PIF4 controls the thermosensory activation of flowering Nature. 484 (7393): pp 242-245.
2012) Studies of Physcomitrella patens reveal that ethylenemediated submergence responses arose relatively early in land-plant evolution Plant Journal. 72 (6): pp 947-959.
2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana Nature. 477 (7365): pp 419-423.
2011) Regenerant Arabidopsis Lineages Display a Distinct Genome-Wide Spectrum of Mutations Conferring Variant Phenotypes Current Biology. 21 (16): pp 1385-1390.
2011) Transient gibberellin application promotes Arabidopsis thaliana hypocotyl cell elongation without maintaining transverse orientation of microtubules on the outer tangential wall of epidermal cells Plant Journal. 69 (4): pp 628-639.
2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: How an "inhibitor of an inhibitor" enables flexible response to fluctuating environments Plant Cell. 21 (5): pp 1328-1339.
2009) High Temperature-Mediated Adaptations in Plant Architecture Require the bHLH Transcription Factor PIF4 Current Biology. 19 (5): pp 408-413.
2008) Plant DELLAs Restrain Growth and Promote Survival of Adversity by Reducing the Levels of Reactive Oxygen Species Current Biology. 18 (9): pp 656-660.
2008) Reduced gibberellin response affects ethylene biosynthesis and responsiveness in the Arabidopsis gai eto2-1 double mutant New Phytologist. 177 (1): pp 128-141.
2008) DELLAs Control Plant Immune Responses by Modulating the Balance of Jasmonic Acid and Salicylic Acid Signaling Current Biology. 18 (9): pp 650-655.
2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis Plant Physiology. 145 (4): pp 1460-1470.