JXB Advance Access published online on February 4, 2008
Journal of Experimental Botany, doi:10.1093/jxb/erm326
REVIEW-ARTICLE |
From plants to animals; the role of plant cell death in ruminant herbivores
Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth SY23 3EB, UK
* To whom correspondence should be addressed. E-mail: alison.kingston-smith{at}bbsrc.ac.uk
Received 7 September 2007; Revised 21 November 2007 Accepted 23 November 2007
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Abstract |
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 Top Abstract IntroductionAbiotic stress-induced cell...Plant-microbe interactions in...Future: options for plant-based...References |
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Plant cell death occurring as a result of adverse environmental conditions is known to limit crop production. It is less well recognized that plant cell death processes can also contribute to the poor environmental footprint of ruminant livestock production. Although the forage cells ingested by grazing ruminant herbivores will ultimately die, the lack of oxygen, elevated temperature, and challenge by microflora experienced in the rumen induce regulated plant stress responses resulting in DNA fragmentation and autolytic protein breakdown during the cell death process. Excessive ruminal proteolysis contributes to the inefficient conversion of plant to microbial and animal protein which results in up to 70% of the ingested nitrogen being returned to the land as the nitrogenous pollutants ammonia and urea. This constitutes a significant challenge for sustainable livestock production. As it is estimated that 25% of cultivated land worldwide is assigned to livestock production, it is clear that understanding the fundamental biology underlying cell death in ingested forage will have a highly significant role in minimizing the impact of human activities. This review examines our current understanding of plant metabolism in the rumen and explores opportunities for exploitation of plant genetics to advance sustainable land use.
Key words: Anoxia, cell death, environment, heat, plant–microbe interactions, proteolysis
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Introduction |
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TopAbstractIntroductionAbiotic stress-induced cell...Plant-microbe interactions in...Future: options for plant-based...References |
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Plant cell death is a major factor determining agricultural productivity. Adverse environmental conditions and infection by microbial pathogens result in loss of biomass and limit maximal crop yields. Considerable plant biomass is also lost as a result of herbivory by vertebrate and invertebrate herbivores and defoliation has been shown to result in nutrient remobilization in response to altered source–sink relationships within the plant (Bakken et al., 1998; Lattanzi et al., 2004). In contrast, little was known about post-ingestion plant cell death until relatively recently when evidence was obtained in support of the hypothesis that the plant metabolism associated with the progression of cell death in ingested tissue affects nutrient utilization by ruminant herbivores (Wallace et al., 2001; Beha et al., 2002; Kingston-Smith et al., 2005b). Commercially, ruminant herbivores require huge amounts of plant biomass, for example, the average dairy cow will consume over 16 tonnes of fresh grass during the grazing season. This represents plant cell death on an enormous scale and, as discussed below, is an important factor in determining the impact of livestock farming on the wider environment (MacRae and Theodorou, 2003).
A major problem for ruminant agriculture is that the conversion of plant to microbial protein is inefficient. As little as 30% of the ingested nitrogen might be retained by the animal for milk or meat production and the non-incorporated nitrogen excreted to the environment as urea or ammonia (MacRae and Ulyatt, 1974; Dewhurst et al., 1996). The source of this inefficiency has been identified as the conversion of plant to microbial protein in the rumen (MacRae and Ulyatt, 1974; MacRae and Theodorou, 2003). The rumen is essentially a large, pH-neutral fermenter. Fermentation of ingested plant particles by the rumen microflora supports microbial growth and the conversion of plant protein to the microbial protein which is digested by the animal further down the digestive tract (Hobson, 1997). Microbial fermentation of plant cell walls generates volatile fatty acids (VFA) which supply energy to support microbial growth, while hydrolysis of peptides generates amino acids which can be deaminated to yield ammonia and VFA (Siddons et al., 1985; Beever and Siddons, 1986; Hobson, 1997). Ammonia can not be taken up by the animal for growth unless first assimilated by rumen micro-organisms. Hence in the scenario where the rate of proteolysis exceeds the relative rate of carbohydrate degradation, ammonia production can exceed the capacity for it to be assimilated by the microbial population and excess is liberated to the environment by the animal as nitrogenous waste (MacRae and Theodorou, 2003). Currently, the European Union is attempting to curb the effects of N pollution through the Water Framework Directive. Full implementation will limit nitrogen release to water with financial penalties for non-compliance. If the efficiency of protein utilization in ruminants can be increased (for instance, by decreasing the rate of protein degradation in the rumen), there will be immediate environmental benefits. To put this into perspective, it is estimated that cattle take in on average 100 kg fresh forage per day at an average composition of 2.5 g N kg–1 (Gibb et al., 1998, 2000). By retaining less than 40% of the N (Dewhurst et al., 1996) this equates to a loss of 150 g N per head of cattle per day, or 54.6 kg per year. The full impact of this can be realized when it is considered that approximately half of the land area of the UK is comprised of improved grassland which supports a UK herd of 8.9 million cattle and 33.5 million sheep (including lambs). Hence, the UK cattle herd alone produces around 1.3 million kg of nitrogenous waste every day. But this is not just a UK–based problem as worldwide grasslands for animal production cover 24% of the earth's vegetated area (Goudriaan, 1995).
Ingested fresh ryegrass can be up to 5 cm in length (AH Kingston-Smith and E-J Kim, unpublished data). It has been estimated by image analysis following vital staining that approximately 50% of the plant cells in ingested plant fragments are viable on entry to the rumen (A Gay, E-J Kim, and AH Kingston-Smith, unpublished results). Although in the past plants have tended to be regarded as passive victims of degradation in the rumen, it is becoming increasingly clear through recent research that control of at least the initial phases of this induced plant cell death process lies with the implementation and co-ordination of plant stress responses. Ingested living plant cells entering the rumen encounter multiple stress signals, probably the most important of which is lack of O2 (Kingston-Smith and Theodorou, 2000). The rumen is a dark, pH-neutral environment, but is maintained at a temperature of 39 °C, thereby producing a simultaneous heat stress. Furthermore, plant tissue will be damaged by ingestive mastication and exposed to a mixed microbial population of bacteria, fungi, protozoa, and methanogens. This is significant as plant tissue may remain in the rumen for up to 24 h until particle size is reduced and residual plant biomass passes into the abomasum which is the site of gastric digestion (Theodorou and France, 1993). Even though the ingested plant material will eventually die, the innate response of the plant cell is to promote chances of surviving periods of non-optimal conditions by adaptation and acclimation to changing environmental conditions. Abiotic stress factors including high and low temperature, excess light, water-logging, and drought are known to result in changes in protein turnover in the field. Hence, sudden exposure of plant cells to abiotic stresses in the rumen (i.e. high temperature, lack of oxygen, prolonged darkness) could also lead to changes in protein turnover and net protein loss (Theodorou et al., 1996; Kingston-Smith and Theodorou, 2000). This realization led to the formation of the hypothesis that plant cells entering the rumen of grazing animals undergo stress-induced cell death which includes autolytic degradation of protein and DNA (Fig. 1; Zhu et al., 1999; Beha et al., 2002; Kingston-Smith et al., 2003a).
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Cell death is fundamental to plant function, defence, and morphology (Jones and Dangl, 1996). Although in some systems ATP concentration can determine whether cell death is programmed (high ATP) or necrotic (low ATP), use as a diagnostic is limited as induction of programmed cell death (PCD) itself can result in low cellular ATP (Vianello et al., 2007). Plant cells undergo cell death in response to developmental processes and environmental stresses. In animal cells, death is orchestrated by the caspase (cysteine-proteases cleaving at an aspartate residue) proteolytic cascade. Evidence for an analogous role for caspases in plants is still lacking, but structural homologues (the metacaspases and vacuolar processing enzymes) have been identified in plants (Hara-Nishimura et al., 2005; Rotari and Gallois, 2005). The vacuolar processing enzymes were initially identified as having a role in the degradation of cellular components during plant defence reactions but have since been identified as caspase homologues and may have a role in programmed cell death (Hara-Nishimura et al., 2005). Both regulatory and degradative proteases are crucial to the breakdown of cellular components by autophagy (mainly in mammalian systems) or autolysis (Beers and McDowell, 2001; Flors et al., 2005). In plants, autolysis can be restricted to loss of nuclear DNA or involve more widespread degradation of cellular components which can continue after cells have died (Beers and McDowell, 2001), thus leading to the suggestion that autolysis in plants may be part of PCD or represent an alternative PCD pathway (Beers and McDowell, 2001).
There is no disputing the fact that rumen microbial enzymes can degrade plant protein (Nugent and Mangan, 1981; Spencer et al., 1981; Nugent et al., 1983), but structural compartmentation of the plant cells and organelles will initially limit access of the microbial proteases to plant protein in newly ingested forage (Cheng et al., 1980; McAllister et al., 1994; Kingston-Smith and Theodorou, 2000; Kingston-Smith et al., 2003b). It is therefore suggested that there is a temporal ecology in the rumen such that stress-induced plant cell death affects the primary colonization behaviour of the rumen microbial community during the first few hours, after which the role of the plant cell becomes more passive as microbial degradation of plant components advances and compartmentation within plant cells is lost. This review considers how exposure of plant cells to the abiotic stresses and micro-organisms present in the rumen affects cell viability, and the consequences of induced plant cell death for proteolysis. By consideration of how stress responses are employed in ingested tissues we can consider our prospects for plant-based manipulation of forage crops to limit environmental pollution.
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Abiotic stress-induced cell death |
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Induced senescence in the rumen?
Senescence is a developmentally regulated cell death programme (Thomas and Stoddart, 1980; Buchannan-Wollaston et al., 2005). Senescence can also be induced by environmental conditions such as drought, lack of nutrients (Thomas and Stoddart, 1980; Kingston-Smith et al., 2005a; Martínez et al., 2007), high temperature (Ferguson et al., 1993), or exposure of excised leaves to prolonged dark (Thimann et al., 1974; Thomas and Stoddart, 1980; Buchannan-Wollaston et al., 2005). Comparison of induction of senescence with exposure of leaves to post-ingestion stresses of the rumen raised the possibility that ingested plant cells undergo an accelerated, induced senescence (Theodorou et al., 1996). Considerable physical change accompanies senescence, including chlorophyll degradation, rearrangement of the thylakoids, and protein remobilization. Chlorophyll breakdown during senescence is an ordered, enzymatic process (Matile et al., 1999) which can be reversed until relatively late (Zaveleta-Mancera et al., 1999), when it enters the terminal cell death phase (Delorme et al., 2000). Limited chlorophyll breakdown can occur over 12 h under rumen conditions (Beha et al., 2002), suggesting that either ATP generation under anoxia is insufficient to support chlorophyll catabolism or that there is insufficient intracellular oxygen to support the action of the oxidases involved (Matile et al., 1999).
During senescence, protein remobilization primarily targets the choroplastic proteins (Thomas and Stoddart, 1980) and is facilitated by induced expression of vacuolar cysteine proteases (Thomas and Stoddart 1980; Smart, 1994; Buchannan-Wollaston, 1997; Delorme et al., 2000). Increased cysteine protease activity is a major characteristic of senescence, but senescence-related expression of the aspartic-, cysteine-, serine-, and metallo-proteases (Guo et al., 2004), and post-translational control of pre-existing proteases (Wiederanders et al., 2003) also occurs. It has been suggested that environmental stress may disrupt normal patterns of protein degradation during senescence (Ferguson et al., 1993), but that the induction of cysteine-proteases culminates in a common degradative pathway (Martínez et al., 2007). During senescence, the main proteolytic capacity resides in the vacuole, with senescence-associated proteases also having been identified in chloroplasts (Andersson and Aro, 1997) and peroxisomes (Distefano et al., 1999). The relevance of protease localization in relation to protein degradation in vivo remains to be fully elucidated. For instance, peroxisomal proteases (for which serine-proteases account for 70% of the activity) are capable of degrading proteins from various cellular compartments, including the chloroplast (Distefano et al., 1999).
The chloroplastic protein Rubisco is highly labile under stress and senescence (Vierstra, 1996; Demirevska-Kepova et al., 2005) and is also a key target for degradation during post-ingestive stress (Zhu et al., 1999; Min et al., 2000; Beha et al., 2002). Stress-induced generation of active oxygen causes modification of amino acids and Rubisco fragmentation (Desimone et al., 1998; Ishida et al., 1998). Ferguson et al. (1993) have suggested that degradation of Rubisco is common to many types of PCD (i.e. biotic or abiotically induced) and may involve signalling by proteases termed saspases (Coffeen and Wolpert, 2004). Saspases are proteases of similar function to caspases but containing an active-site serine residue instead of cysteine (Coffeen and Wolpert, 2004). In situ labelling studies have shown that during exposure to rumen-like stress there is a decrease in intensity of Rubisco label in chloroplasts (Beha et al., 2002), suggesting that Rubisco is broken down within the chloroplasts. The protease(s) responsible for this degradation have not yet been identified, although it is possible for Rubisco degradation to be completed either within or outside the chloroplast (i.e. requiring transport of holoenzyme or peptide subunits to cytoplasm or vacuole). Stromal proteases active against Rubisco have been identified in pea (Robinson and Ellis, 1984; Bushnell et al., 1993), and Rubisco can also be degraded in the cytoplasm via the energy-demanding Clp proteases (Liu and Jagendorf, 1984) or the proteasome–ubiquitin system (Veierskov and Ferguson, 1991). Ubiquitin–proteasome-mediated proteolysis has a broad range of substrates and its main role is considered to be in nitrogen recycling during senescence, heat shock, and wounding (Belknap and Garbarino, 1996). It has been suggested that ubiquitin-mediated proteolysis also has a role as a negative effector of PCD (Schologelhofer et al., 2006) and in the regulation of signalling cross-talk under a number of environmental stresses as well as following pathogen attack (Dangl and Jones, 2001). In the context of the rumen, the potential of ATP-requiring systems could be limited by restricted energy generation under anoxia (see ‘Effect of anoxia on plant cells in the rumen’). However, while some comparisons of senescence and post-ingestion autolysis can be made, there are differences. For example, while both senescence and in vitro heat/anoxic stress cause nitrogen remobilization in white clover (Kingston-Smith et al., 2005a, 2006), the two conditions result in different profiles of protease activity, notably lacking up-regulation of senescence-associated cysteine-proteases under anoxia and elevated temperature.
Heat stress in the rumen
Temperate crop plants can encounter temperatures of 35–40 °C (Wise et al., 2004). Therefore while the rumen temperature of 39 °C will represent a heat stress for most forage crops, it is one to which they will respond while attempting to survive the stress until the return to ambient conditions. An increase in temperature of 1 °C for 1 h can cause heat shock and induce both up- and down-regulation of gene expression (Busch et al., 2005), while exposure to temperatures above 35 °C results in net loss of protein, changes in chloroplast morphology, and organization of photosynthetic proteins, but with little or no loss of chlorophyll (Rokka et al., 2001; Vani et al., 2001; Beha et al., 2002; Tang et al., 2007). Heat stress can induce a number of symptoms of apoptotic PCD in plant cells including activation of a caspase-3-like protease and cleavage of poly (ADP-ribose) polymerase (PARP; Tian et al., 2000). PARP is associated with DNA repair in viable cells, but is inactivated by the action of caspase-3 during apoptosis. Apoptosis results in intra-nucleosomal strand breaks in nuclear DNA which can be resolved as ‘ladders’ on agarose gels. Heat stress has been shown to induce DNA laddering and Rubisco proteolysis (Coffeen and Wolpert, 2004) while cells subjected to rumen-like stresses also show apoptotic like strand breaks in the DNA (Kingston-Smith et al., 2003a). The combination of preservation of intracellular structure (Beha et al., 2002) and evidence for control of the cell death process suggests that ingested cells are reacting to the combined stresses in a defined, non-necrotic way. Although this exhibits characteristics of apoptosis, reported differences in PCD between plants and animals (Hara-Nishimura et al., 2005; Rotari and Gallois, 2005) indicate that programmed cell death in plants is significantly different from the process occurring in animals.
The primary characteristic following exposure to heat shock is the synthesis of heat shock proteins (Hsp). Hsp are found in each cellular compartment and represent a class of chaperonin which are described according to molecular size (Sun et al., 2002; Wang et al., 2004; Lee et al., 2007b). Synthesis of Hsp under stress is thought to protect pre-existing protein against damage and enables refolding of damaged proteins (Wang et al., 2004). The chloroplast located small heat shock proteins (sHsp) are involved in assisting rather than direct re-folding (Lee et al., 2007b), particularly in promoting the correct folding of Rubisco (Houtz and Portis, 2003). Therefore, it is possible that the environmental stress encountered in the rumen results in an inability to synthesize or correctly fold newly synthesized Rubisco, causing the observed net loss of Rubisco protein during 12 h in vitro incubation (Beha et al., 2002; Kingston-Smith et al., 2003a).
Synthesis of Hsp is regulated by transcription of heat stress factors (HSF; reviewed in Miller and Mittler, 2005; Kotak et al., 2007). Despite their name, HSF can affect a broad range of pathways associated with tolerance to biotic and abiotic stresses (Busch et al., 2005). The heat shock response can be further regulated by ubiquitin (Mathew et al., 1998; Ferreira et al., 2006) and signalling by plant hormones including jasmonates (Kotak et al., 2007). Jasmonates are membrane-lipid-derived signalling molecules associated with development and stress responses (Wasternack, 2007). Changes in membrane permeability as a result of subjecting leaves to anoxia and elevated temperature (Kingston-Smith et al., 2003b) suggest that lipid-based signalling compounds could be involved in heat-stress-mediated proteolysis and cell death in ingested plant cells.
Effect of anoxia on plant cells in the rumen
Forage crops have evolved in an aerobic environment in which oxygenic ATP generation by the mitochondria drives cellular processes and growth. Although development of metabolic adaptations have given rise to genotypic differences in tolerance to anoxia (Crawford and Braendle, 1996; Vartapetian et al., 2003; Perata and Voesenek, 2007), plant growth is severely limited by the absence of oxygen, for instance, during periods of flooding. Globally this is estimated to affect about 16% of the area used for production (Huynh et al., 2005). Physical adaptation of plants to waterlogging includes the formation of aerenchyma which are cells in the roots or shoots which have been modified by programmed cell death to contain large gas spaces (Evans, 2003). Aerenchyma are formed in response to a number of abiotic stresses including hypoxia, high temperature, and drought, but surprisingly they can not be formed under full anoxia (Igamberdiev et al., 2005; Thomas et al., 2005).
Under full anoxia, for instance after prolonged flooding, cell death can result from insufficient ATP generation, accumulation of the fermentation products ethanol or acetaldhehyde, or cytoplasmic acidosis (Vartapetian and Jackson, 1997). Lack of oxygen affects respiratory electron transport and, in the absence of oxygen, ethanolic fermentation produces only 2 ATP per glucose molecule as compared with 32 by oxidative phosphorylation. In maize roots, there appears to be a regulatory relationship between build-up of cytoplasmic lactate and pH-mediated induction of pyruvate decarboxylase to facilitate the metabolic switch between respiration and fermentation (the Roberts–Davies model; Davies et al., 1974; Roberts et al., 1984), but evidence from other species and organs is less supportive of this elegant theory (Tadege et al., 1998; Felle, 2005). Exposure of leaf discs to low oxygen conditions in an in vitro simulation of the rumen environment results in a rapid decline in ATP in leaf discs and a concomitant rise in cellular ethanol consistent with this model (Fig. 2). The fermentation intermediate acetaldehyde accumulates during periods of low oxygen (Pfister-Sieber and Braendle, 1994), even when ethanol concentrations are minimal (Rahman et al, 2001). Acetaldehyde is toxic to the cell as it is an electron donor thereby achieving the apparent paradox of enabling generation of reactive oxygen species under anoxia (Mustroph et al., 2006). Reactive oxygen molecules perform a signalling role and are the source of cellular damage to proteins and lipids depending on the extent of accumulation (Noctor and Foyer, 1998; Rahman et al., 2001).
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Interestingly, in in vitro simulations of rumen exposure, although lack of oxygen leads to rapid depletion of foliar ATP, this does not appear to fall completely to zero, even after many h of exposure to rumen-like conditions (Fig. 2). Potentially, this low supply of ATP can be used to support de novo synthesis of the anaerobic response proteins (ARP) which can be expressed as little as 90 min after the onset of anoxia (Sachs et al., 1996; Dat et al., 2004). Synthesis of the ARP is essential to maintaining structure and function of cells under anoxia (Vartapetian et al., 2003) and this is regulated by the anaerobic response element (ARE; Dolferus et al., 1994). As with HSF, ARE sequences are not necessarily specific to low oxygen sensing, but can be induced in response to other abiotic stresses including low temperature and wounding (Dolferus et al., 1994, 1997).
Anoxia promotes irreversible physical changes in mitochondria and chloroplasts. Mitochondrial swelling, changes in membrane composition and irreversible membrane damage can occur within 2 h of exposure to anoxia (Crawford and Braendle, 1996; Vartapetian et al., 2003) or when the rate of ATP synthesis falls below 10 µmol g–1 fresh weight h–1 (Rawyler et al., 1999). Prolonged anoxia (24–48 h) results in what appears to be an energy-demanding disassembly of the mitochondrial structure (Vartapetian et al., 2003). Therefore, while changes in membrane permeability do occur under simulated rumen conditions (Kingston-Smith et al., 2003b), the observation that chloroplasts appear to remain intact during up to 8 h exposure (Beha et al., 2002) probably reflects differences in the relative stabilities of the tonoplast and chloroplast membranes under the heat/anoxia stress combination.
Exposure of leaf sections to in vitro simulation of rumen conditions results in proteolysis and, specifically, the generation of a Rubisco breakdown product of approximately 45 kDa (Beha et al., 2002; Kingston-Smith et al., 2003a). It is not known at present if this is the same as the peptide generated under anoxia when approximately 10–15 kDa is removed from the large subunit (Mitsuhashi et al., 1992; Hildbrand et al., 1994), apparently mediated by a cysteine-protease cleaving after glutamate at position 14 (Navarre and Wolpert, 1999). Mitsuhashi et al. (1992) have suggested that accumulation of the high molecular weight breakdown products of Rubisco under anoxia could represent a block in the Rubisco breakdown pathway because further steps require O2. An alternative explaination is that further steps require ATP and it is ATP limitation under anoxia which limits complete remobilization of the N reserves held in Rubisco. Hildbrand et al. (1994) found no incorporation of 35S-methionine in leaf discs incubated under N2, indicating that proteolysis under anoxia was mediated by pre-existing proteases. Anoxia-induced remobilization of nitrogen reserves could fulfil a protective role with nitrate and nitrite acting as electron acceptors thereby limiting generation of radicals and cellular damage (Igamberdiev et al., 2005; Libourel et al., 2006).
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Plant–microbe interactions in the rumen |
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Microbial colonization of ingested plant particles
Rumen micro-organisms become attached to ingested particles very quickly post-ingestion with rumen bacterial DNA being detected on plant particles within 5 min of exposure to the rumen microbiota (Koike et al., 2003; Edwards et al., 2007). Quantitative PCR combined with molecular fingerprinting techniques has confirmed that this result is not due to significant contamination of leaf surfaces by epiphytic bacteria (Edwards et al., 2007) and proliferation of bacteria under rumen-like conditions is only observed when a rumen inoculum has been introduced (Fig. 3). For comparison, rumen content was estimated to contain approximately 730 µg bacterial DNA g–1 dry matter (JE Edwards, unpublished results). Although motile bacteria can respond chemotactically to find their substrate, for example, to a carbohydrate signal, the role(s) of these primary colonizers and their relationship with micro-organisms involved in secondary phases of colonization remains to be elucidated. Vital staining has shown that cell death is not uniform when leaf discs are exposed to rumen micro-organisms, but is largely restricted to areas of damage where bacteria can actively invade weakened cells or proliferate in intercellular spaces (Cheng et al., 1980; Fig. 4). Although entry via stomata is possible, exposure to dark conditions and high CO2 concentrations will promote stomatal closure. The lack of a regular pattern of invasion on leaf discs shows stomatal access to be, if anything, a minor component of microbial attack of ingested tissues over 6 h (Fig. 4). This is in agreement with recent evidence from Melotto et al. (2006) who have shown that stomata close within 2 h of detection of the microbial pathogens.
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Under field conditions, leaves are regularly exposed to pathogenic bacteria and fungi and have evolved defence systems to minimize damage. These include gene-for-gene resistance, the hypersensitive response (HR) and systemic acquired resistance (SAR) which have been excellently reviewed elsewhere (Greenberg, 1997; Tadege et al., 1998; Heath, 2000; Dangl and Jones, 2001). A successful virulent reaction requires active involvement by the host, active protein synthesis and may even co-opt the plant defence reaction (e.g. by stimulating the production of hydrogen peroxide early in programmed cell death signalling) to enhance colonization (Howlett, 2006). In defence against pathogens, plant cells require energy to enable specific changes in gene expression to facilitate de novo protein expression (Katagiri, 2004), and the generation and secretion of antimicrobial compounds such as oxylipins (Prost et al., 2005), peptides (Broekaert et al., 1997) and protease inhibitors (Abe et al., 1987) to inhibit colonization. Recent evidence indicates that the rumen microbial ecosystem is composed of 300–400 different species of bacteria (Edwards et al., 2004; Yu et al., 2006). Currently, 18 species of ruminal anaerobic fungi have been identified using cultivation-based approaches (Ho and Barr, 1995; Chen et al., 2002; Dehority, 2003; Chen et al., 2007), although, based on recent molecular-based techniques, it appears that the actual number of species that exist is likely to be significantly higher (Tuckwell et al., 2005). Therefore, it is possible that at least some of these micro-organisms (or their secreted secondary metabolites) can be recognized by the plant cells as potentially invasive. Based on our understanding of plant–microbe interactions during virulent and avirulent aerobic microbial challenges, it is reasonable to suspect that plant cells are unlikely to be passive during colonization by rumen micro-organisms.
Pathogen-induced cell death and regulation of defence reactions
Pathogenic micro-organisms can produce secondary metabolite toxins which directly promote cell death in their host (Howlett, 2003). Proteinaceous fungal elicitors (e.g. endoxylanases and elicitins) stimulate defence reactions recruiting lipid (Shah, 2005; Belien et al., 2006) and mitogen-activated protein kinase (MAPK) signalling pathways (Zhang et al., 2006) to promote localized cell death. The fungus Colchliobolus victoriae produces the toxin victorin which promotes a form of programmed cell death in oat during victoria blight infection (Coffeen and Wolpert, 2004). Exposure to victorin promotes Rubisco degradation, but this could be prevented by use of caspase- and general protease inhibitors (Coffeen and Wolpert, 2004). The proteinaceous fungal elicitor cryptogein has been shown to induce transcription of the 20S subunit of the 26S proteasome complex (Dahan et al., 2001), thereby increasing the availability of peptides from the plant host to the colonizing micro-organisms. Although it is possible that elicitor-like substances are present in the rumen it is not yet clear if they are a significant factor in induction of autolytic cell death. While it is accepted that the primary role of microbial colonizers is in cell wall degradation to provide energy for microbial growth (Theodorou and France, 1993), the role of micro-organisms in protein degradation has been questioned following results from both in vitro and in sacco experimentation which have shown similar levels of protein degradation in the presence and absence of rumen fluid (Zhu et al., 1999; Kingston-Smith et al., 2005b). This observation, combined with evidence that the result is not due to microbial contamination of leaf surfaces (Fig. 3), indicates that the microbial contribution to in vitro proteolysis is minimal, but that the role of the microbial enzymes is in the generation of amino acids from peptides, suitable for assimilation by the microbial population (Zhu et al., 1999; Wallace et al., 2001; Kingston-Smith et al., 2005b).
The plant genome contains resistance factors (R) that permit recognition of specific pathogen-derived avirulence factors (avr). Interaction between these plant and microbial factors initiates HR and SAR via the accumulation of salicylic acid (SA) and redox-mediated conformational changes in NPR1 (Heath, 2000; Mou et al., 2003). Of the plant defence responses, HR is of particular interest here because of the ability of ‘resistant’ plants to mount a defence following attack by certain, normally pathogenic micro-organisms; the plant induces cell wall changes and a localized region of cell death to both limit nutrient availability to the pathogen and form a physical barrier to further penetration into the leaf. Pathogenic attack of leaf tissue stimulates increased cellular production of salicylic acid which, via the NPR1 regulatory protein, induces synthesis of PR1 (pathogenesis related protein 1; Yu et al., 2001). Synthesis of PR1 in white clover leaf discs exposed to a rumen population (AH Kingston-Smith, unpublished results) indicates that plant cells do put up an active defence against the microbiota within the rumen. Hence, the plant's ability to mount defence reactions during colonization by rumen micro-organisms could also modulate the onset of plant cell death in ingested plant particles. Again, the extent to which defence proteins can be synthesized will depend on the energy available under conditions of restricted ATP generation under anoxia.
Exposure to virulent micro-organisms results in expression of defence-associated genes (Katagiri, 2004). Many of these genes appear to be generic for biotic stress rather than being expressed in response to individual pathogens. For instance, although SA and JA-mediated signalling pathways are involved in achieving resistance of Arabidopsis to the bacterial pathogen Pseudomonas syringae and the necrotrophic fungal pathogen Alternaria brassicicola, about half of the genes involved are common to both reactions, supporting the idea of signal convergence during defence reactions (Katagiri, 2004) possbily co-ordinated via the WRKY transcription factors (Yu et al., 2001; Zheng et al., 2006). Microbial challenge to plant tissues could be modulated indirectly by the products of unrelated stress responses. For instance, recent evidence suggests that herbivory can induce protection against some bacterial pathogens, exploiting the multiple roles of JA in stress signal transduction (De Vos et al., 2006). Furthermore, changes in lipid metabolism as a result of innate defence reactions or anoxic stress could contribute to promoting or inhibiting microbial attack on ingested plant cells (Shah, 2005). Of the unsaturated fatty acids present in plant tissues, linolenic acid (18:3) is a precursor of jasmonic acid, but this is decreased in tissue held under anoxia as fatty acids become saturated (Shah, 2005; Lee et al., 2007a), thereby increasing the potential for microbial colonization as defence reactions are suppressed.
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Future: options for plant-based strategies |
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It is clear that in order to improve the environmental sustainability of livestock farming there is a real need to identify the relationships between the plant genome and its impact on rumen function. Particularly important is the elucidation of the mechanism underlying the control of the plant cellular response when multiple stress signals are imposed, and the impact of these stress responses for microbial colonization. Therefore, the most immediate target will be to understand how we can limit plant-mediated proteolysis by altering the way cells die in response to the rumen stress, a combination of heat/anoxic/biotic stress (Kingston-Smith and Thomas, 2003).
Naturally occurring variation in abundance and activity of proteases with season and plant species (Kingston-Smith et al., 2003c, 2005a; Shaw, 2005; Pichard et al., 2007) provides genetic diversity from which to selectively breed improved forage varieties. However, caution should be taken about simply aiming to decrease the total protease activity in plants which could potentially leave forage crops more susceptible to pathogen attack in the field. Furthermore, this approach may not be as successful as predicted because, to date, it has not been possible to correlate total protease activity with extent or rate of autolytic protein degradation. This could be due to a fundamental feedback control sensing cytoplasmic amino acid concentrations being overcome by diffusion from damaged cell membranes (Kingston-Smith et al., 2003c, 2006; Shaw 2005). A more directed approach could target serine proteases. Serine proteases have been shown to be up-regulated in response to rumen stress in white clover (Kingston-Smith et al., 2006) and Pichard et al. (2007) concluded that serine proteases were the most abundant form in non-senescent forage crops. An alternative approach to protein protection would be to modulate the occurrence of secondary compounds (such as tannins or phenolic complexes) to preseve protein once placed under ingestive stress (Lee et al., 2007a), or to target the signal transduction pathway culminating with proteolysis.
Therefore, future research should address identification of key plant traits governing onset and progression of cell death-associated proteolysis. Recent development of farm-scale models (del Prado and Scholefield, 2006) will permit the effectiveness of potential traits to be tested in silico. This will enable the focused generation of molecular and biochemical markers appropriate to selective breeding of improved forage crops by exploitation of techniques in marker-assisted selection and introgression hybridization (Kingston-Smith and Thomas, 2003; Shaw, 2005; King et al., 2007).
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Acknowledgements |
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The authors would like to thank all the students, current and former members of staff who have contributed to the study of plant-mediated autolysis at IGER Aberystwyth. The secretarial assistance of Jessica Longworth during the preparation of this manuscript is greatly appreciated. The authors are funded by the Biotechnology and Biological Sciences Research Council (BBSRC), UK.
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