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Altering the Cell Wall and Its Impact on Plant Disease: from Forage to Bioenergy

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Altering the Cell Wall and Its Impact on Plant Disease: from Forage to Bioenergy PY52CH04-Dixon ARI 4 July 2014 16:28 Altering the Cell Wall and Its Impact on Plant Disease: From Forage to Bioenergy Qiao Zhao1 and Richard A. Dixon2,3,∗ 1Plant Biology Division, Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401; email: [email protected] 2Department of Biological Sciences, University of North Texas, Denton, Texas 76203-5017; email: [email protected] 3US Department of Energy, BioEnergy Sciences Center (BESC), Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831 Annu. Rev. Phytopathol. 2014. 52:69–91 Keywords First published online as a Review in Advance on forage quality, lignin modification, oligosaccharin, plant-pathogen defense, May 9, 2014 secondary cell wall The Annual Review of Phytopathology is online at phyto.annualreviews.org Abstract This article’s doi: The individual sugars found within the major classes of plant cell wall poly- by ${individualUser.displayName} on 08/07/14. For personal use only. 10.1146/annurev-phyto-082712-102237 mers are dietary components of herbivores and are targeted for release in Copyright c 2014 by Annual Reviews. Annu. Rev. Phytopathol. 2014.52:69-91. Downloaded from www.annualreviews.org industrial processes for fermentation to liquid biofuels. With a growing un- All rights reserved derstanding of the biosynthesis of the complex cell wall polymers, genetic ∗ Corresponding author modification strategies are being developed to target the cell wall to improve the digestibility of forage crops and to render lignocellulose less recalcitrant for bioprocessing. This raises concerns as to whether altering cell wall prop- erties to improve biomass processing traits may inadvertently make plants more susceptible to diseases and pests. Here, we review the impacts of cell wall modification on plant defense, as assessed from studies in model plants utilizing mutants or transgenic modification and in crop plants specifically engineered for improved biomass or bioenergy traits. Such studies reveal that cell wall modifications can indeed have unintended impacts on plant defense, but these are not always negative. 69 PY52CH04-Dixon ARI 4 July 2014 16:28 INTRODUCTION Lignocellulosic biomass drives forage-based milk and meat production and is also emerging as Liquid biofuel: a feedstock for the production of liquid biofuels after processing to release cell wall sugars for a liquid fuel, such as fermentation. Limitations (collectively termed recalcitrance) inherent in the properties of ligno- ethanol or isobutanol, cellulosic materials negatively impact both forage utilization (49) and processing of biomass for generated by biofuels (53); recalcitrance restricts access of enzymes to the cellulose microfibrils and also prob- fermentation of sugars released from biomass ably to hemicelluloses, which together represent the major polysaccharide components of both primary and secondary cell walls (Figure 1). These polymers contain the hexose and pentose Recalcitrance: apropertyofplantcell sugar units that must be released for either animal nutrition (in the rumen) or fermentation to walls that restricts ethanol or other liquid biofuels (in the biofuel refinery). Although the phenomenon of cell wall access to enzymes for recalcitrance is complex, the presence of the phenylpropanoid polymer lignin in secondary cell deconstruction of cell walls contributes a major barrier to cell wall deconstruction (69). This contention is supported wall polysaccharides by detailed studies of cell wall structures during digestion by fungal and bacterial cellulases (28), Hemicellulose: as well as by the fact that genetic modification to reduce lignin levels or alter lignin composition a group of results in improved digestibility of forages (21, 49) and in increased soluble sugar and fermentable heteropolymeric cell wall matrix ethanol yields from bioenergy crops, such as switchgrass (Panicum virgatum L.) (41, 106). polysaccharides, such Strong cell walls evolved as a critical feature in enabling early plants to colonize the land. As as xylans and an upright growth habit became necessary to allow plants to outcompete each other for access arabinoxylans, present to sunlight above the foliar canopy, mechanical strength of stems became paramount. It also in almost all plant cell became critical to maintain hydrophobicity of conducting vessels for efficient transpiration, and walls lignin, which provides both hydrophobicity and mechanical strength, fulfilled this role admirably. Secondary cell wall: Plants also had to protect their cell walls from penetration by bacterial and fungal pathogens a thick layer rich in lignin formed inside seeking access to the nutrient-rich environment within the cell. Recalcitrance has therefore evolved the primary cell wall over millennia to support plant structure and defense. The plant cell wall is dynamic, and both when it has stopped its structure and composition change during pathogenesis, partly as a result of modification by increasing in surface microbial wall–degrading enzymes (28) and partly as a result of induced defenses that are targeted area at the wall (124). It therefore seems logical that our attempts to improve plants for agriculture and Lignin: an abundant other industrial purposes might interfere with the outcome of interactions with microbes. phenylpropanoid This review addresses the relationships between plant cell wall structure and defense from polymer found primarily in plant different but related perspectives. First, we provide a brief overview of the modifications to cell secondary cell walls wall structure that appear to function as inducible defense responses. The major part of the and produced by the review then focuses on the impacts of cell wall modification on defense, covering studies in model oxidative systems, such as Arabidopsis, and work aimed directly at reducing recalcitrance in forage and by ${individualUser.displayName} on 08/07/14. For personal use only. polymerization of bioenergy crops. Much of this information has become available since the last review on the cell p-hydroxycinnamyl alcohols (monolignols) wall and plant defense in this series (54). Potential mechanisms linking cell wall modification to Annu. Rev. Phytopathol. 2014.52:69-91. Downloaded from www.annualreviews.org plant defense are presented, and recent strategies for balancing reduced recalcitrance with optimal plant performance are outlined. CHANGES IN THE CELL WALL DURING PLANT DEFENSE Plant pathogens actively attack cell walls using enzymatic tools (63), and sometimes physical force (118), to gain access to intracellular nutrients. Cell wall–associated plant defense is therefore spatially a first line of defense and is not a static barrier. Rather, plants respond dynamically to pathogen attack at the level of the cell wall through pathogen-triggered lignification (129, 139), deposition of the β1,3-glucan callose (75), structural alterations to cell wall polysaccharides (135), production of reactive oxygen species (65, 90), protein cross-linking (13), and biosynthesis and deposition of antimicrobial compounds (phytoalexins) (3) (Figure 1). Many of these features of induced defense are closely associated with formation of papillae within the cell wall at the site of 70 Zhao · Dixon PY52CH04-Dixon ARI 4 July 2014 16:28 Lignin biosynthesis Plant with engineered CH2OH HO Monolignols, cell wall (naïve) MeO lignans, and Callose deposition Induced lignification conjugates Signal transduction pathways ? H2O2 H2O2 Hormonal PR imbalance proteins Signal transduction Lignin biosynthesis Pathogen pathways CH2OH HO Wild-type plant Pathogenesis (primary wall) MeO Plasma membrane PR proteins HO O H Plasma membrane O H O O Phytoalexins Cell wall Cytoplasm Cytoplasm Cell wall Cellulose microfibril Callose Hemicellulose Oligogalacturonide receptor Lignin Cell wall-degrading enzyme Intact pectin Pathogen-associated by ${individualUser.displayName} on 08/07/14. For personal use only. molecular pattern (PAMP) Pectic fragment (oligogalacturonide) (DAMP) PAMP receptor Annu. Rev. Phytopathol. 2014.52:69-91. Downloaded from www.annualreviews.org Figure 1 Scheme showing common responses to pathogen infection at the cell wall level and how similar responses may occur in uninfected plants following modifications to cell wall components, particularly lignin. Left panel: Pathogen-induced responses. Right panel (top): Constitutive responses in a plant in which lignin levels and degree of polymerization in secondary cell walls have been reduced through mutation or genetic manipulation of a monolignol pathway gene. Significant differences may exist in the responses of different species, or in the same species, dependent on the site of downregulation. Right panel (bottom): Wild-type plant. Abbreviations: DAMP, damage-associated molecular pattern; PR, pathogenesis-related. Broad arrows (red and purple) represent specific receptor-linked signal pathways; thin black arrows represent downstream biochemical pathways. www.annualreviews.org • Altering the Cell Wall 71 PY52CH04-Dixon ARI 4 July 2014 16:28 attempted penetration (124). Not only do lignins play a role as physical barriers against infection, but the unpolymerized monolignol building blocks of lignins may themselves have antimicrobial activity (5, 7, 54). Furthermore, as discussed in more detail below, cell wall–degrading proteins Pectin: a water-soluble produced by pathogens can release host cell wall materials (such as oligogalacturonides released polysaccharide from from pectin) that may be perceived by plants as signals for the activation of defense responses
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