Streptomyces scabies

At least four other species of Streptomyces also cause diseases on potato tubers.[7] The most widespread species other than S. scabies are S. turgidiscabies and S. acidiscabies, which can be distinguished based on their morphology, the way they utilise food sources and their 16S RNA sequences.[1] Unlike S. scabies, S. acidiscabies is predominantly seed-borne rather than soil-borne and be suppressed using insecticides and nematicides, suggesting that microfauna play a role in its transmission.[11] In 2003 three other species of Streptomyces that cause common scab symptoms were isolated in Korea and named S. luridiscabiei, S. puniciscabiei and S. niveiscabiei. They differ from S. scabies by having spores that are of different colours.[12] S. ipomoea causes a similar disease on sweet potato tubers.[13]

There are also other species of Streptomyces found in scab lesions on potato tubers that do not cause disease. 16 distinct strains have been isolated from tubers and based on a genetic analysis of them, they are most similar to S. griseoruber, S. violaceusniger, S. albidoflavus and S. atroolivaceus.[14]

There are other microbes that cause similar damage to potato crops to S. scabies. In the UK the most common are the powdery scab caused by the protist Spongospora subterranea f. sp. subterranea and silver scurf and black dot caused by the fungi Helminthosporium solani and Colletotrichum coccodes respectively.[17] Netted scab is thought to be caused by other species including S. reticuliscabiei.[18]

Five toxins have been isolated from S. scabies that induce the formation of scabs on potato tubers. They are classed as 2,5-Diketopiperazines,[20] with the most abundant having the chemical formula C₂₂H₂₂N₄0₆. The first two to be isolated in 1989 were thaxtomin A and thaxtomin B, of which thaxtomin A was the predominant compound. Thaxtomin A and thaxtomin B differ only by thaxtomin B having a hydrogen at C₂₀ rather than a hydroxyl group.[21] Three years later the same group of researchers isolated several other toxins with similar structures to the first two they had isolated[22] which are thought to be precursors to thaxtomin A.[23] Thaxtomin A is considered to be essential for symptoms to appear[24] and the pathogenicity of strains is correlated with the amount of thaxtomin A they produce.[25] It is synthesised by a protein synthetase encoded by the txtA and txtB genes, forming a cyclic dipeptide which is then hydroxylated by a cytochrome P450 monooxygenase encoded by txtC. The dipeptide is then nitrated by an enzyme similar to mammalian nitric oxide synthase[24] at the four position on the tryptophan residue.[26] All the genes required for thaxtomin biosynthesis are located on one part of the genome, termed the pathogenicity island, that is also found in S. acidiscabies and S. turgidiscabies[24] which is around 660 kb in length.[26] The toxins are only produced once the bacteria have colonised a potato tuber and it is thought they detect potatoes by sensing certain molecules present in their cell walls. Cellobiose, a subunit of cellulose, activates thaxtomin production in some strains, but suberin also acts as an activator, causing many changes to the proteome of the bacteria after it is detected.[24]

The target of the toxins is unknown but there is evidence that they inhibit the growth of plant cell walls.[7] They are neither organ or plant specific and if added to the leaves of various species cause them to die,[27] indicating that the target is highly conserved.[28] Adding thaxtomin A to seedlings or suspended plant cell cultures causes them to increase in volume and onion root tips treated with it are unable to form cell plates suggesting that it affects the synthesis of cellulose. Inhibiting the production of cell walls may aid S. scabies in penetrating plant cells, a key step in infection. The fact that scabs only form in regions of rapidly growing tissue is consistent with this hypothesis.[7]

As well as genes that produce toxins, other genes have been identified which help S. scabies to infect plants. A tomatinase enzyme, encoded by tomA which can degrade the antimicrobial saponin α–tomatine. The aerial growth of mutants lacking the gene is inhibited, but the mycelium is able to continue to grow.[29] Nec1 is another protein that is required for virulence, which is secreted out of the bacteria. It is not clear how it leads to disease, but it may suppress the defense mechanisms that thaxtomin activates.[30] Another gene cluster in the 87.22 strain is very similar to a cluster found in the Gram negative plant pathogens Pseudomonas syringae and Pectobacterium atrosepticum. The cluster produces coronafacic acid, part of the plant toxin coronatine which mimics the plant hormone jasmonate, contributing to virulence.[28]

In 2007 the transcriptional regulator txtR was identified which is a member of the AraC/XylS protein family. The protein detects cellobiose and then causes changes in gene expression of the genes required for thaxtomin production, as well as the production of txtR. When txtR is silenced in the 87.22 strain, the expression of txtA, txtB and txtC decreases 40 fold resulting in a dramatic decrease in thaxtomin A production. TxtR is not the universal regulator of pathogenicity however as some nec1 and tomA are not affected by silencing it. It is thought that S. scabies cannot degrade cellulose itself and that instead it detects cellobiose that leaks through plant cell walls at areas where the roots are actively growing.[26]

The twin-arginine translocation pathway is an important pathway involved in virulence, which transports proteins through the cell membrane of the bacteria. Over 100 different proteins are thought to be transported by the pathway, some of which are required for virulence, but others just for normal growth.[28]

Very little is known about the defense mechanisms that plants use against actinobacteria such as S. scabies. When the model plant, Arabidopsis thaliana is challenged by S. scabies or thaxtomin A it produces the antimicrobial phytoalexin called scopoletin, which is known to accumulate in tobacco when it is infected by pathogens. This leads to the bacteria growing more slowly and producing less thaxtomin A, thought to be linked to the repression of the nitric oxide synthase gene involved in its synthesis. Scopoletin has been detected in diseased potato tubers, but its role in the defense against S. scabies is unknown. Other defense mechanisms have also been noted in A. thaliana to thaxtomin A, including the initiation of programmed cell death, an efflux of hydrogen ions and an influx of calcium ions.[27]

Streptomyces scabies can infect many plants, but is most commonly encountered causing disease on tuber and tap root crops. It causes common scab on potato (Solanum tuberosum), beet (Beta vulgaris), carrot (Daucus carota), parsnip (Pastinaca sativa), radish (Raphanus sativus), rutabaga (Brassica napobrassica) and turnip (Brassica rapa). It also inhibits the growth of the seedlings of both monocot and dicot plants.[1] Potato varieties differ in their susceptibility to S. scabies.[11] More resistant varieties tending to have fewer, tougher lenticels and a thicker skin, although authors do not agree on the specific characteristics required for resistance.[19]