Chapter Nine - Applications of transgenic approaches in developing an understanding of drought tolerance in poplar

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Abstract

This paper will present an overview of genetic approaches to develop an understanding of interacting roles of reduced nitrogen in conferring drought tolerance in poplar. Included in the discussion are: (1) the critical role that drought tolerant phenotypes of forest trees will play in a worldwide environment faced with the challenges of climate change; (2) a summary of transgenic technologies as applied to poplar with assessment of recent transgenic approaches into biological mechanisms for drought tolerance; and (3) the relationship between nitrogen assimilation and drought tolerance in poplar. Inherent in this discussion is assessment of the complexity and pleiotropic nature of drought tolerant phenotypes, including physiological, biochemical, morphological, and genetic components (Allwright & Taylor, 2016; Borland et al., 2015; Harfouche, Meilan, & Altman, 2014; Polle & Chen, 2015). Central to this discussion are the considerable advances in poplar biology and genome analysis resulting in defining poplar as a model forest species (Bradshaw, Ceulemans, Davis, & Stettler, 2000; Cronk, 2005; Taylor, 2002). Focus is not only on the application of GE technologies for expression of specific transgenes to produce new phenotypes, but also on assessment of specific phenotypes created through GE approaches that can allow identification of specific genes and gene expression networks correlated with the induced phenotype that can be incorporated into advanced breeding approaches.

Section snippets

The need for drought tolerant energy crops, including poplar

The current worldwide environment is facing significant challenges directly associated with increased release of heat-trapping greenhouse gases. These changes have not only resulted in areas with significant increases in the occurrences of drought, but predictions of long term increase in global mean temperatures (IPCC, 2014; Walsh et al., 2014). Moreover, if the trend continues, increases in global temperatures will result in changing precipitation patterns reflected in drought in certain

Agrobacterium transformations

Instrumental to genetic improvement of energy crops are applications of evolving biotechnology. These approaches pose significant opportunities for improvement of important agronomic traits of forest species including enhanced biomass production and drought and salt tolerance (for reviews: Dinneny et al., 2008; Dubouzet, Strabala, & Wagner, 2013; Polle, Janz, Teichmann, & Lipka, 2013; Wang, Cai, Xu, Wang, & Dai, 2016; Wang, Liu, et al., 2016; Yadav, Ayre, & Bush, 2015). Both forward and reverse

What transgenic technologies have revealed about drought tolerance in poplar

A number of recent reports describe efforts to enhance drought tolerance in poplar using GE technology. These reports reveal underlying biological factors and genetic contributions to this important trait. The reports summarized below focus on three major areas that contribute to this important phenotype in poplar: enhanced ability of drought resistant phenotypes to reduce the effects of drought-induced reactive oxygen species, ABA responses on stomatal behaviour and tissue patterning related

Nitrogen utilization in trees and the central role of glutamine synthetase

The availability of inorganic nitrogen in soils is often a limiting factor in plant growth and development. Most tree species grow in areas where nitrate and/or ammonium are the major forms of nitrogen available in soil (Wolt & Wolt, 1994).

One main difference between herbaceous and woody plants is the manner by which soil nitrate is assimilated. In many tree species the majority of nitrate taken up from soil is reduced in roots to ammonium by the action of both nitrate reductase (NR) and

The relationship between nitrogen assimilation and drought tolerance in hybrid poplar

Recognizing the importance of developing an understanding of drought tolerance, we have investigated mechanisms for enhanced drought tolerance observed in GS poplar in ecophysiological studies (El-Khatib et al., 2004; Molina-Rueda & Kirby, 2015; Molina-Rueda et al., 2013; Zhong et al., 2004). In comparison to leaves of WT controls, GS poplars maintain expression of fundamental enzymes (GS, GOGAT, and Rubisco) under water stress and during recovery. Overexpression of GS also sustained

Conclusions

An overview of the applications of genetic engineering approaches to develop an understanding of interacting roles of reduced nitrogen in conferring drought tolerance in poplar is presented. Overexpression of glutamine synthetase (GS) causes alterations to nitrogen metabolism including higher production of free amino acids including glutamine, glutamate, and GABA. In addition to contributing to enhanced growth, these metabolites can act as signals driving changes in expression of stress-related

Acknowledgements

We gratefully acknowledge the efforts of the laboratory of Dr. Chung Jui Tsai at the University of Georgia for patient collaboration on the poplar transcriptome analysis and expression network analysis.

References (113)

  • A.G. Good et al.

    Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production?

    Trends in Plant Science

    (2004)
  • R.E. Häusler et al.

    Plant science amino acids—A life between metabolism and signaling

    Plant Science

    (2014)
  • J.J. Molina-Rueda et al.

    Transgenic poplar expressing the pine GS1a show alterations in nitrogen homeostasis during drought

    Plant Physiology and Biochemistry

    (2015)
  • M. Pagliai et al.

    Soil structure and the effect of management practices

    Soil and Tillage Research

    (2004)
  • M. Pascual et al.

    Response of transgenic poplar overexpressing cytosolic glutamine synthetase to phosphinothricin

    Phytochemistry

    (2008)
  • B.J. Shelp et al.

    Hypothesis/review: Contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress

    Plant Science: An International Journal of Experimental Plant Biology

    (2012)
  • B.J. Shelp et al.

    Compartmentation of GABA metabolism raises intriguing questions

    Trends in Plant Science

    (2012)
  • H.C. Thomsen et al.

    Cytosolic glutamine synthetase: A target for improvement of crop nitrogen use efficiency?

    Trends in Plant Science

    (2014)
  • M. Wang et al.

    New insight into the strategy for nitrogen metabolism in plant cells

    International Review of Cell and Molecular Biology

    (2014)
  • L. Wang et al.

    Differential expression profiles of poplar MAP kinase kinases in response to abiotic stresses and plant hormones, and overexpression of PtMKK4 improves the drought tolerance of poplar

    Gene

    (2014)
  • R.G. Alscher et al.

    Role of superoxide dismutases (SODs) in controlling oxidative stress in plants

    Journal of Experimental Botany

    (2002)
  • M. Andrews et al.

    Can genetic manipulation of plant nitrogen assimilation enzymes result in increased crop yield and greater N-use efficiency? An assessment

    Annals of Applied Biology

    (2004)
  • C. Avila et al.

    Spatial and temporal expression of two cytosolic glutamine synthetase genes in Scots pine: Functional implications on nitrogen metabolism during early stages of conifer development

    Plant Journal

    (2001)
  • D. Bauer et al.

    A role for cytosolic glutamine synthetase in the remobilization of leaf nitrogen during water stress in tomato

    Physiologia Plantarum

    (1997)
  • P.H. Beatty et al.

    Transcriptome analysis of nitrogen-efficient rice over-expressing alanine aminotransferase

    Plant Biotechnology Journal

    (2009)
  • S.M. Bernard et al.

    The importance of cytosolic glutamine synthetase in nitrogen\assimilation and recycling

    The New Phytologist

    (2009)
  • M. Betti et al.

    Glutamine synthetase in legumes: Recent advances in enzyme structure and functional genomics

    International Journal of Molecular Sciences

    (2012)
  • A. Blum

    Crop responses to drought and the interpretation of adaptation

    Plant Growth Regulation

    (1996)
  • C. Boisvenue et al.

    Impacts of climate change on natural forest productivity—Evidence since the middle of the 20th century

    Global Change Biology

    (2006)
  • M. Bor et al.

    Comparative effects of drought, salt, heavy metal and heat stresses on gamma-aminobutryric acid levels of sesame (Sesamum indicum L.)

    Acta Physiologiae Plantarum

    (2009)
  • A.M. Borland et al.

    Climate-resilient agroforestry: Physiological responses to climate change and engineering of crassulacean acid metabolism (CAM) as a mitigation strategy

    Plant, Cell and Environment

    (2015)
  • H.D. Bradshaw et al.

    Emerging model systems in plant biology: Poplar (Populus) as a model forest tree

    Journal of Plant Growth Regulation

    (2000)
  • V.B. Busov et al.

    Genetic transformation: A powerful tool for dissection of adaptive traits in trees

    New Phytologist

    (2005)
  • V. Castro-Rodríguez et al.

    The glutamine synthetase gene family in Populus

    BMC Plant Biology

    (2011)
  • M. Civelek et al.

    Systems genetics approaches to understand complex traits

    Nature Reviews. Genetics

    (2014)
  • H.D. Coleman et al.

    Enhanced expression of glutamine synthetase (GS1a) confers altered fibre and wood chemistry in field grown hybrid poplar (Populus tremula X alba) (717-1B4)

    Plant Biotechnology Journal

    (2012)
  • M. Coque et al.

    Genomic regions involved in response to grain yield selection at high and low nitrogen fertilization in maize

    Theoretical and Applied Genetics

    (2006)
  • Q.C.B. Cronk

    Plant eco-devo: The potential of poplar as a model organism

    New Phytologist

    (2005)
  • L.J. Cseke et al.

    High efficiency poplar transformation

    Plant Cell Reports

    (2007)
  • F. De la Torre et al.

    Functional expression of two pine glutamine synthetase genes in bacteria reveals that they encode cytosolic holoenzymes with different molecular and catalytic properties

    Plant and Cell Physiology

    (2002)
  • Y. Demirci et al.

    CRISPR/Cas9: An RNA-guided highly precise synthetic tool for plant genome editing

    Journal of Cellular Physiology

    (2018)
  • J.R. Dinneny et al.

    Cell identity mediates the response of Arabidopsis roots to abiotic stress

    Science (New York, N.Y.)

    (2008)
  • B. Dombrecht et al.

    MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis

    The Plant Cell

    (2007)
  • Z. Du et al.

    agriGO: A GO analysis toolkit for the agricultural community

    Nucleic Acids Research

    (2010)
  • R.T. El-Khatib et al.

    Transgenic poplar characterized by ectopic expression of a pine cytosolic glutamine synthetase gene exhibits enhanced tolerance to water stress

    Tree Physiology

    (2004)
  • E. Elorriaga et al.

    Variation in mutation spectra among CRISPR/Cas9 mutagenized poplars

    Frontiers in Plant Science

    (2018)
  • D. Fan et al.

    Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation

    Scientific Reports

    (2015)
  • B.G. Forde et al.

    Glutamate in plants: Metabolism, regulation, and signalling

    Journal of Experimental Botany

    (2007)
  • C.H. Foyer et al.

    Understanding oxidative stress and antioxidant functions to enhance photosynthesis

    Plant Physiology

    (2011)
  • F. Gallardo et al.

    Expression of a conifer glutamine synthetase gene in transgenic poplar

    Planta

    (1999)

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