A web site designed to provide links to information on metabolic pathways in potato (Solanum tuberosum) including disease resistance, drought responses (to Dicots and Monocots), Arabidopsis signaling etc (see Downloads section for all PDFs available).
One problem for plant scientists is that many of the metabolic pathway diagrams which are available commercially are actually describing reactions which occur in microbes or animal systems rather than being plant specific. An additional problem for plant pathologists is that information on metabolic pathways usually refers to healthy tissues and does not include information on secondary metabolites associated with resistance. Also, whilst many processes are common between different plant species, the chemistry of those responses is different between families. Thus it is not possible to draw a single unifying pathway that will describe events in all plants. Over the last decade Gary Lyon has produced a number of diagrams showing the metabolic pathways of diseased potatoes and these have been updated as new information has been published. The latest available version of the chart (dated 28 October 2013) can be downloaded as a PDF from here:- Metabolic Pathways of the Diseased Potato.
[There are more diagrams in the Download section, including:- Arabidopsis signalling, ceramide signalling, cysteine metabolism, glutamine / glutamate pathways, nuclear events associated with disease resistance, phosphoinositide cascade, plant drought responses, ROS and nitric oxide, SUMO and ubiquitin ].
The chart was drawn using information derived only from refereed published papers and contains information on the biosynthesis of many compounds that are associated with disease resistance and shows the complexity of the plant's response to infection (Lyon, 1997a; Lyon 1997b). A list of the references used as a source of information to construct the chart can also be downloaded:- chart references. Secondary metabolites such as the anthocyanins pelargonidin and peonidin are not included in the pathway diagram as there is no evidence that they are associated with disease resistance in potato.
The Metabolic Pathways of the Diseased Potato diagram is best viewed as a wall-mounted poster.
A small part of the Metabolic Pathways of the Diseased Potato PDF has been made into a jpg and shown on the left to indicate the type of information available in the chart.
A PDF of the ceramide signalling pathway can be downloaded from the 'Downloads' section.
A number of publications have suggested a role for ceramide signalling in programmed cell death in plants. For example, Liang et al. (2003) proposed a role for ceramide phosphorylation modulating cell death in plants.
Murphy et al. (2008) provided evidence of a role for inositol hexakisphosphate in the maintenance of basal resistance to plant pathogens. Mosblech et al. (2008) suggested a role for phosphoinositide signalling in mediating plant wound responses.
An A4 size PDF of the phosphoinosite cascade can be downloaded from the 'Downloads' section.
Plant scientists are currently placing more emphasis on identifying genes that are either up- or down-regulated upon infection using potato microarrays. Some of these genes, such as WRKY transcription factors (Dellagi et al., 2000), will be involved in early signalling events that are still poorly characterised and are currently more difficult to place on a metabolic pathway. A review of WRKY transcription factors in plants has been published by Rushton et al. (2010) and the role of WRKY transcription factors in plant immunity has been described by Pandey and Somssich (2009). Techniques for identifying potato genes differentially regulated by plant pathogens such as Phytophthora infestans and Erwinia carotovora (more recently classified as Pectobacterium atroseptica) have been described by Birch et al. (1999) and Dellagi et al. (2000).
Information recently added to the chart
Information obtained from the following publications has been used to add additional information to the metabolic pathways chart over the last year or so:-
Kaschani et al. (2010) showed that the papain-like cysteine protease C14 in potato is a common target of EPIC1 and EPIC2B, two apoplastic cystatin-like proteins secreted by P. infestans.
King & Calhoun (2010) described the identification of a feruloyltyramine trimer, as a potential suberin intermediate, which was isolated from potato common scab lesions.
Serra et al. (2010) published information on feruloyl transferases involved in suberin biosynthesis in potato. They showed that silencing the feruloyl transferase in potato affected normal skin maturation and caused the formation of conjugated polyamines.
Li et al. (2009) used cDNA-AFLP to identify potato genes differentially expressed by application of DL-β-amino-butyric acid which induced resistance to subsequent inoculation with P. infestans. They noted that some differentially expressed transcript derived fragments were homologous to genes encoding proteins related to jasmonic acid and salicylic acid dependent signalling pathways.
Baebler et al. (2009) used potato TIGR microarrays to monitor the expression of potato genes at 0.5 or 12h after inoculation of a resistant and a susceptible cultivar to Potato Virus YNTN. They identified a number of genes with an altered transcript abundance in response to the virus including genes associated with photosynthesis, perception, signalling and defence.
Tian et al. (2006) used cDNA microarrays to investigate Phytopthora infestans induced genes in potato leaves with horizontal resistance.They used an array containing 100 ESTs, from a subtractive cDNA library, of which 76 were differentially expressed in infected plants compared to controls. The results indicated that multiple defense mechanisms are involved in horizontal resistance to late blight and alteration in metabolic pathways is one of the most important defense responses.
Tian et al. (2010) described a C2H2-type zinc finger protein gene, StZFP1, which was induced in potato by salt, dehydration and ABA, and was also responsive to infection by P. infestans.
Gao et al. (2009) reported the isolation of the nonspecific lipid transfer protein StLTPa7 which was upregulated in potato by Ralstonia solanacearum and the gene was also stimulated by salicylic acid, methyl jasmonate, abscisic acid and calcium.
Wu et al. (2009a) described the isolation of a Solanum tuberosum ankyrin repeat gene (Star) from potato leaves challenged by Phytophthora infestans. Star encodes a RING finger repeat protein, a putative E3 ubiquitin ligase.
A leucine-rich repeat receptor-like protein kinase gene StLRPK1 was induced in potato leaves by P. infestans and showed different profiles after treatment with salicylic acid, methyl jasmonate, ethylene, abscisic acid, wounding, 40 degrees C and salinity stress (Wu et al. 2009b).
A RING-H2 finger protein gene, StRFP1, is constitutively expressed in potato leaves but is significantly induced by P. infestans, abscisic acid, salicylic acid and methyl jasmonate (Ni et al., 2010). Ni et al. suggested that StRFP1 contributes to broad spectrum resistance to P. infestans in potato.
Manosalva et al. (2010) identified the potato ortholog of tobacco SABP2 (StMES1) and showed that the recombinant protein converts methyl salicylate to salicylic acid. Further, they showed that potato plants in which StMES1 activity was suppressed were compromised for arachidonic acid-induced systemic acquired resistance (SAR).
van den Berg and Takken (2010) described a role for SUMO conjugation in regulating plant innate immunity.
Chanda (2011) showed that glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants.
Ma et al. (2011) published information on the role of bZIP11 which is involved in regulating carbohydrate metabolism, including T6P and SnRK1, in Arabidopsis. (TheT6P gene is up-regulated by P. infestans in potato).
Koo et al. (2011) showed that in Arabidopsis the cytochrome P450 CYP94B3 is involved in controlling the level of the plant hormone jasmonate-L-isoleucine through negative feedback. JA-Ile signals through the COI1-JAZ coreceptor complex in Arabidopsis.
Bakker et al. (2011) identified the presence of 280 TIR-NB-LRR and 448 CC-NB-LRR sequences in Solanum tuberosum ssp. tuberosum.
van Verk et al. (2011) showed that in Arabidopsis AtWRKY28 and AtWRKY46 are transcriptional activators of ICS1 (isochorismate synthase)and PBS3 (AVRPPHB SUSCEPTIBLE 3) respectively. This is a strong indication of how these genes may be regulated in potato.
Gallou et al. (2011) used microarray and real-time qPCR to detect transcriptome changes during pre-, early and late stages of potato root colonization by Glomus sp MUCL 41833. They showed up-regulation of a number of genes including allyl alcohol dehydrogenase and a number of WRKY genes.
Orłowska et al. (2011) looked at differentially expressed transcript derived fragments in a resistant and a susceptible potato cultivar inoculated with Phytopthora infestans. Most of the genes studied showed different expression profiles between the cultivars.
Alvarez et al. (2012) highlighted the important role of cysteine in plant immunity in Arabidopsis.
González-Lamothe et al. (2008) described the activation of PR10a by Why1 and the negative regulation of PR10a by SEBF in potato.
Senthil-Kumar and Mysore (2012) showed that ornithine delta-aminotransferase and proline dehydrogenases are involved in defence against nonhost pathogens in Arabidopsis and Nicotiana benthamiana.
El Hadrami et al. (2011) detected 2-protocatechuoylphloroglucinolcarboxylic acid (2-PCPGCA) in potato infected with Verticillium dahliae. They suggested that V. dahliae dioxygenally oxidised quercetin to form 2-PCPGCA.
Henriquez et al. (2012) used HPLC to quantify seconday metabolites' profiles in potato leaves in response to various isolates of P. infestans. They identified catechin, flavonol-glucoside, flavonone, rutin, and a terpenoid.
Aliferis and Jabaji (2012) identified azelaic acid (amongst many other compounds) in potato sprouts infected with Rhizoctonia solani. (Azelaic acid has previously been reported to prime Arabidopsis to accumulate salicylic acid).
Saunders et al. (2012) showed that the putative plant phosphatase BSU-LIKE PROTEIN1 (BSL1) is required for R2-mediated perception of AVR2 and resistance to P. infestans and AVR2 associates with BSL1 and mediates the interaction of BSL1 with R2 in planta.
Engelhardt et al. (2012) showed that effector recognition and subsequent HR requires R3a relocalization to vesicles in the endocytic pathway.
Kim et al. (2013) described the isolation from potato tubers of a peptide G2 (PG-2) possessing antimicrobial activity including activity against Clavibacter michiganensis subsp. michiganensis, and also described the earlier isolation of potamin-1 (PT-1), a 5.6-kDa trypsin-chymotrypsin protease inhibitor.
McLellan et al. (2013) showed that the RxLR effector PITG_03192 (Pi03192) prevents CF-triggered re-localisation of StNTP1 and StNTP2 from the ER into the nucleus.
Information on potatoes not yet included in Metabolic Pathways diagram
Lindqvist-Kreuze et al. (2010) used the TIGR 10k potato array and real-time RT-PCR to compare the response of Solanum cajamarquense and an advanced tetraploid clone B3C1 after inoculation with P. infestans. All data are publicly available in the Solanaceae Gene Expression Database at ftp://ftp.tigr.org/pub/data/s_tuberosum/SGED as study number 83.
Henriquez and Dayyf (2010) used subtractive hybridization and cDNA-AFLP to identify differentially expressed genes involved in the potato-P. infestans interaction. Genes included some that were potentially controlling pathogenesis or avr genes in P. infestans as well as those potentially involved in potato resistance.
El Bazaoui et al. (2011) described the identification by GC/MS of a number of tropane alkaloids from Datura stramonium. Some of these compounds may therefore be present in potato as D. stramonium is also a member of the Solanaceae.
Scherer et al. (2010) have reviewed the nomenclature and function of patatin-related enzymes in plants. Patatins are potato tuber proteins with acyl-hydrolyzing activity.
Eschen-Lippold et al. (2012) showed that transgenic potato plants with reduced expression of SYNTAXIN-RELATED1 (StSYR1) showed spontaneous necrosis and chlorosis in later stages of development. They showed that enhanced resistance of StSYR1-RNAi plants to Phytophthora infestans correlated with enhanced salicylic acid levels whereas levels of 12-oxophytodienoic acid and jasmonic acid were unaltered.
Other interesting references on resistance
Bartsch et al. (2010) provided evidence for the existence of 2,3-dihydroxybenzoic acid (2,3-DHBA) whose accumulation depends on EDS1 in resistance responses and during ageing in Arabidopsis. They also showed that 2,3-DHBA exists predominantly as a xylose-conjugated form (2-hydroxy-3-β-O-D-xylopyranosyloxy benzoic acid). Bartsch et al. also describe the presence of 2,5-DHBA2-O-β-D-glucoside and 2,5-DHBA5-O-β-D-glucoside which are synthesised from 2,5-DHBA. These conjugates have not yet been isolated from potato.
Goyer (2010) described the biosynthetic pathway of thiamine in plants. Thiamine is involved as a cofactor in response to biotic and abiotic stress in plants.
Melech-Bonfil & Sessa (2010) showed that SIMAPKKKe is a signalling molecule that positively regulates cell death networks associated with plant immunity in tomato. By suppressing the expression of various MAPKK and MAPK genes and overexpressing the SIMAPKKKe kinase domain they identified a signalling cascade acting downstream of SIMAPKKKe that includes MEK2, WIPK and SIPK.
Oh et al. (2010) showed that a 14-3-3 protein, TFT7, was required for PCD (which required MAPKKK alpha) in tomato, and was associated with resistance to Pseudomonas syringae pv tomato.
Spaepen and Vanderleyden (2010) suggested that down-regulation of auxin signaling (in bacteria) is part of the plant defence system against phytopathogenic bacteria, and exogenous application of auxin eg produced by the pathogen, enhances susceptibility to the bacterial pathogen.
Qi et al. (2010) describes the signalling cascade initiated by AtPeps which leads to the expression of pathogen defense genes in a calcium dependent manner in Arabidopsis.
Cecchini et al. (2011) describes the role of proline dehydrogenase in Arabidopsis showing it is involved in defence against pathogens.
Yun et al. (2011) described the role of S-nitrosylation of NADP oxidase in regulating cell death in plant immunity in Arabidopsis.
Choi et al. (2012) showed that in Capsicum annuum PR10 interacted with a leucine-rich repeat protein (LRR1) and the PR10-LRR1 complex is essential for cell death mediated defence signalling.
Kobayashi et al. (2012) studied the expression and interaction of StCDPK5VK and StRBOHA-D. They showed that transgenic potato plants, expressing StCDPK5 under the control of a pathogen-inducible promoter, showed resistance to the near-obligate hemibiotrophic pathogen P. infestans and, by contrast, increased susceptibility to the necrotrophic pathogen A. solani.
Wu et al. (2012) showed that the Arabidopsis protein NPR1 is a receptor for salicylic acid.
The Metabolic Pathways chart also highlights compounds such as ethylene, salicylic acid, jasmonic acid, oligogalacturonides, arachidonic acid, linolenic and linoleic acids which induce some of the resistance-related responses when applied exogenously to potato (see Walters et al., 2005 and Walters, Newton & Lyon, 2007 for a review of induced resistance in plants). Elicitor-active oligogalacturonides bind to wall associated kinase (WAK1) (for example Cabrera et al., 2008).
Freeman & Beattie (2008) have published an overview of plant defenses against pathogens and herbivores which is available on the web and includes some information about potato. A more specific article on induced resistance in potato is available here.
Eschen-Lippold et al. (2010) showed that transgenic potato plants impaired in either the 9-lipoxygenase pathway (which produces defence-related compounds) or the 13-lipoxygenase pathway (which generates jasmonic acid-derived signals) still expressed BABA-induced resistance. However, plants unable to accumulate salicylic acid failed to show BABA-induced resistance demonstrating the importance of a functional salicylic acid pathway for systemic resistance in potato induced by BABA (beta amino butyric acid).
A recent report by Soleimani & Kirk (2012) described the application of several resistance inducers (ASM, chitosan, salicylic acid and Heads-up) on potato to control brown leaf spot disease caused by Alternaria alternata.
Machinandiarena et al. (2012) showed that potassium phosphite primed the defence response of potato to P. infestans and that expression of StNPR1 and StWRKY1 was enhanced in response to the phosphite.
Arasimowicz-Jelonek et al. (2012) analysed the proteome response of potato leaves to β-aminobutyric acid (BABA), γ-aminobutyric acid (GABA), laminarin, 2,6-dichloroisonicotinic acid (INA), and S-nitrosoglutathione.
Chaturvedi et al. (2012) described dehydroabietinal, an abietane diterpenoid, as a potent activator of systemic acquired resistance in Arabidopsis.
Chen et al. (2013) showed that showed that the GH3.5 protein in Arabidopsis could catalyze the conjugation of SA with aspartic acid to form SA-Asp and that SA-Asp could induce PR gene expression and increase disease resistance to pathogenic Pseudomonas syringae.
Li & Dhaubhadel (2010) reviewed 14-3-3 proteins in soybean and described the existence of 18 14-3-3 genes of which 16 are transcribed making this the largest family of 14-3-3 proteins described in plants to date.
Abiotic stress responses e.g. to drought, are still poorly characterised and are covered in more detail in a separate page of the web site; see Drought. Some information on the abiotic stress response of Arabidopsis, which was obtained from the DRASTIC (Database Resource for the Analysis of Signal Transduction in Cells at www.drastic.org.uk) gene expression database is available on that page.
The image on the right shows an output from DRASTIC showing Arabidopsis genes up-regulated (in red) or down-regulated (in blue) by ABA, cold, drought or sodium chloride.
A PDF showing metabolic pathways associated with drought responses in plants (Dicots) is also available (this is being up-dated regularly).
Shao et al. (2011) provided a mini review of aminopropyltransferases in plants. (Spermidine and spermine are synthesized in plants by aminopropyltransferases). Interestingly, these authors suggested that "often there is a poor correlation among transcripts, enzyme activity and cellular contect of the respective polyamine".
A schematic diagram of the biosynthetic pathway for anthocyanins, caffeoylquinates, and other major phenolic derivatives in potato tuber has been published by Stushnoff et al. (2010).
Lecourieux et al. (2006) review the role of calcium in plant defence-signalling pathways. This is not specific to potato but is describing plants in general.
A diagram showing the carotenoid biosynthesis pathway in potato has been published by Diretto et al. (2006).
Combinatorial biosynthesis is the process by which novel natural products can be generated by combining metabolic pathways from different organisms through genetic means. For example, this can be particularly useful for producing medicinal products of high value. Julsing et al. (2006) provide a useful review on this subject giving specific examples and outlining future potential. Pollier et al. (2011) provide a more recent review of the potential for combinatorial biosynthesis involving plants.
Reyes et al (2011) reviewed endosomal trafficking pathways in plants and described its role in biosynthetic pathways. They included information on the trans-Golgi network (TGN), the retromer, the ADP-ribosylation factor (ARF), and the endosomal sorting complexes required for transport (ESCRTs).
Grotewold (2006) reviewed the biosynthesis, regulation and contribution to flower colour of anthocyanins (part of the flavonoid pathway), carotenoids (derived from isoprenoids) and betalains (derived from tyrosine). This review deals with plants in general and is not specific to potato.
Ohyama et al. (2013) provided evidence on the biosynthesis of steroidal alkaloids in the Solanaceae.
MicroRNAs are post-transcriptional expression regulators that act on their target genes by degradation of target mRNAs or by inhibition of target protein translation (Xie et al., 2010). Xie et al. (2010) have reviewed the role of microRNAs in potato and identified 202 potential potato miRNAs. They also identified / predicted 1094 miRNA targets. Tang (2010) has provided a review of plant microRNAs. Kim et al. (2011) identified 22 miRNAs and 221 target genes in potato.
Katiyar-Agarwal and Jin (2010) described the role of small RNAs in host-microbe interactions. They discussed pathogen-regulated host microRNAs and small interfering RNAs (siRNAs), and introduced small RNA pathway components including Dicer-like proteins (DCLs), double stranded RNA (dsRNA) binding protein, RNA-dependent RNA polymerases (RDRs), small RNA methyltransferase HEN1, and Argonaute (AGO) proteins, that contribute to plant immune responses.
Zhang et al. (2011) showed that Arabidopsis argonaute 2 regulates immunity via miRNA393(*)-mediated silencing of a golgi-localised SNARE gene MEMB12.
Small RNAs (sRNAs; 20-24 nucleotides long) are involved in abiotic stress responses.
Wan et al. (2011) used computational techniques to identify 16 drought stress-associated miRNA families in Physcomitrella patens. They constructed a miRNA co-regulation network, and identified two network hubs miR902a-5p and miR414. Their data is available via an on-line database named ppt-miRBase.
Ivashuta et al. (2011) describe the regulation of gene expression in plants through miRNA inactivation suggesting that endogenous miRNA decoys may have an important role in modulating gene expression in plants.
Zhou et al. (2010) described 30 microRNAs which were either up- or down-regulated in rice in response to drought stress.
Li et al. (2012) demonstrated a conserved role for miRNAs and secondary siRNAs in NB-LRR/LRR immune receptor gene regulation and pathogen resistance in tobacco, tomato and potato.
Zhang et al. (2013) used high throughput sequencing to identify 28 conserved miRNA families and identified potato-specific miRNAs which were identified and validated by RNA gel blot hybridization.
Dynamic nuclear trafficking between cytoplasm and nucleus is becoming recognised as an important aspect influencing plant metabolism. Liu & Coaker (2008) discussed evidence implicating nucleo-cytoplasmic trafficking in plant disease resistance as mutations in nucleoporins and importins can compromise resistance signalling. A more recent review of the importance of nucleo-cytoplasmic trafficking has been published by Deslandes & Rivas (2011).
Regulation and manipulation of nucleotide metabolism in plants has been reviewed by Zrenner et al. (2006).
The oxylipin biosynthetic pathway in potato is shown in the Metabolic Pathways of the Diseased Potato. In addition, Florian Brodhun and Ivo Feussner have provided a useful summary of oxylipin biosynthetic pathways in plants. Koo and Howe (2012) described the catabolism and breakdown of jasmonyl-isoleucine in Arabidopsis and provide very useful information on related compounds (a similar system, and the same compounds, is likely to be functioning in potato).
Hanke et al. (2012) published useful information on inositol phosphate composition of potato leaves and identified pathways of inositol phosphate metabolism.
Stulemeijer & Joosten (2008) reviewed the different types of post-translational modification that play a role in plant immunity including phosphorylation, glycosylation, ubiquitination,sumoylation, nitrosylation, myristoylation, palmitoylation and glycosylphosphatidylinositol (GPI)-anchoring. Cysteine glutathionylation of kinases may be an important general machanism of kinase regulation (Anselmo & Cobb, 2004) - this has been described as occurring in animal systems but may also occur in plants. Burg & Takken (2010) discussed SUMO-, MAPK-, and resistance protein-signaling in relation to plant immunity and suggested that SUMO conjugation could transform transcription activators into repressors. Briggs and Bent (2011) reviewed poly(ADP-ribosylation) via poly(ADP-ribose) polymerases (PARPs) and poly(ADP-ribose) glycohydrolases (PARGs) which are involved with certain biotic and abiotic stress responses - these enzymes have been implicated in programmed cell death. Bourque et al. (2011) showed that type-2 nuclear histone deacetylases (HDACs) act as negative regulators of elicitor-induced cell death in tobacco suggesting that HR is controlled by post-translational modifications including (de)acetylation of nuclear proteins. Vierstra (2012) reviewed the role of ubiquitin and ubiquitin-like modifiers.
Chivasa et al. (2013) identified proteins associated with PCD in Arabidopsis and showed that UDP-glucose pyrophosphorylase 1 (UGP1), a sucrose-induced gene, is a critical factor that regulates fumonisin B1-induced PCD.
Sequence information on the potato genome has been published (2011). Potato Genome Sequencing Consortium. Nature Paper. Jupe et al. (2012) identified 438 NB-LRR type genes in a phureja clone of potato. Of those predicted genes 77 contained a TIR-like domain, and 107 of the remaining 361 non-TIR genes contained an N-terminal coiled-coil (CC) domain.
Jupe et al. (2013), using resistance gene enrichment sequencing (RenSeq), increased the number of identified NB-LRRs from 438 to 755.
Ambrosome et al. (2012) review the current knowledge of RNA-binding proteins in plants, their role in plant metabolism and response to abiotic stress, and state that more than 200 RBPs have been predicted in Arabidopsis and rice genomes.
Ghillebert et al. (2011) reviewed the structure, function and regulation of the AMPK/SNF1/SnRK1 complex in different organisms. In plants SnRK1 is thought to be activated by energy-depleting stress conditions thereby controlling normal growth and a variety of cellular processes. SnRKs are associated with ABA and drought responses. In Arabidopsis 38 SnRKs have been identified which are divided into the 3 subgroups SnRK1, SnRK2 and SnRK3 (Hrabak et al., 2003).
Confraria et al. (2013) suggested that miRNAs are components of the SnRK1 signaling cascade contributing to the regulation of specific mRNA targets
A diagram showing the sucrose breakdown pathway in the potato tuber has been published by Weise et al. (2006)
Singh et al. (2013) carried out a genome-wide analysis of SNAC transcription factors in potato and identified 110 StNAC genes encoding for 136 proteins. Some of these genes, including StNAC072 and StNAC101 that are orthologs of known stress-responsive Arabidopsis genes eg RD26, were identified as highly abiotic stress responsive.