Overview

Phytophthora alni Brasier & S.A. Kirk (2004) was discovered in 1993 in southern England causing lethal root and collar rot in alders. It has subsequently been reported in many European countries including the Netherlands, Germany, France, Sweden, Belgium, Austria and Hungary, and has recently been found in Alaska and Oregon. P. alni is unusually variable, perhaps as a result of recent hybridizations among related species. There are three subspecies: the most commonly isolated and most virulent subspecies P. alni ssp. alni and two less commonly isolated subspecies, P. alni ssp. uniformis and P. alni ssp. multiformis. Etymology: From Alnus, the tree from which the pathogen was first isolated.

Morphology

The typical form of P. alni, P. alni ssp. alni, is homothallic, with gametangia usually frequent. Oogonia have tapered stalks, and are variably warty with bullate protuberances (similar to those of P. cambivora). Diameters of mature oogonia commonly range from 43 to 50 um. Other oogonia are only partially developed and sometimes distorted or with beak-like or tube-like projections. Commonly many oogonia abort or produce thin-walled oospores. Antheridia are predominantly two-celled and amphigynous. Sporangia are not seen on carrot agar (CA) but are produced sparsely in pea broth or when plugs from margins of actively growing cultures on CA are partially submerged in pond water or soil leachate. Sporangia are borne singly on long sporangiophores, ellipsoid, non-papillate, and noncaducous. They exhibit nested or extended internal proliferation. Average sporangial lengths range from 48–60 mm and widths range from 31 to 43 mm. The length/width ratio ranges from about 1.3 to 1.6. No chlamydospores are observed. The other subspecies of P. alni are recognizably similar to P. alni ssp. alni, but are often more variable in growth and morphology. Many isolates appear to be unstable in culture.

Genetics

Phytophthora alni is in phylogenetic clade 7, with its evident ancestor, P. cambivora. A recent genetic analysis has suggested that P. alni alni. was generated on many separate occasions by the hybridization of either P. alni uniformis with P. alni multiformis or their ancestors. The same analysis suggests that P. alni uniformis may have P. cambivora as an ancestor. P. alni multiformis may have been generated by autopolyploidization (the spontaneous duplication of chromosome number within a species) or by ancient hybridization of two unknown species. Unlike most species of Phytophthora, which are diploid, P. alni alni is near tetraploid and unable to complete meiosis beyond metaphase I. In culture, many oogonia prematurely abort or appear abnormal and only one third of the oospores that appear normal are reported to be viable. As a result it is believed to spread predominantly via asexual means, namely zoospores produced in sporangia.

Growth

Colonies growing on carrot agar (CA) are usually appressed-felty with no or very sparse aerial mycelium; sometimes they are appressed with a little uniform woolly overgrowth close to the colony surface. Colonies sometimes have faster or slower growing areas. Optimum temperature for growth on CA is about 23–25 °C. The upper limit for growth on CA is about 29 °C. Radial growth at 25 °C on CA ranges from 4 to 8 mm/d.

Distinguishing characteristics for identification

Phytophthora alni appears similar to P. cambivora in colony form with bullate oogonia and 2-celled antheridia. P. alni is homothallic, however. The fluffy, patternless colony morphology on agar is distinctive. Sporangia are usually slow to form, and not abundant. They are non-papillate and generally non-descript.

The searchable web-based database phytopthora-id.org is useful for rapid identification of Phytophthora species based on sequencing of the ITS or Cox spacer regions, followed by BLAST searching the database. The database includes only sequences that are associated with published Phytophthora species descriptions or classic Phytophthora phylogenetics references.

Q-bank (comprehensive databases on regulated plant pests, based in the Netherlands) offers identification of unknown Phytophthora specimens with the help of any combination of morphological and molecular data. www.q-bank.eu

Disease History

In 1993 an unusual Phytophthora was first isolated from bark lesions on the lower boles of dying alders along waterways in Britain. The Phytophthora resembled P. cambivora in both its gametangial and sporangial morphology. However, it was homothallic and many oogonia aborted. An inoculation test confirmed its pathogenicity to Alnus. It has subsequently been reported in most European countries and a subspecies of the pathogen has recently been found in Alaska and Oregon. P. alni consists of three subspecies, the most commonly isolated and most virulent subspecies P. alni ssp. alni (also referred to as the 'standard form') and two less commonly isolated subspecies P. alni ssp. uniformis (also called the Swedish variant) and P. alni ssp. multiformis (which contains the Dutch, German and UK variants).

Impacts in the Forest

Phytophthora disease of alder is now widespread in Europe in the riparian ecosystems where alder commonly grows. It is also damaging alder in forest plantations, especially in Germany. In England, disease incidence is highest in the southeast, but heavy losses are also occurring in some of the large alder populations in western England and parts of Wales. The disease is also causing damage to alders on Scottish river systems, including the Rivers Avon, Dee, Deveron, Duirinish and Spey. Outside the UK, alder disease is now widespread in Europe with very high losses in northeastern France and Bavaria in Germany; in other areas disease impact is not yet so serious. Until 2006 the alder Phytophthora had not been found outside Europe, but recent reports suggest that a similar pathogen is present in a nursery in Minnesota, USA, infecting a woody ornamental species and in wildland streams in Alaska and Oregon. Interestingly, in Alaska and Oregon the pathogen was recovered from soil, not trees, and although isolates are pathogenic in artificial inoculation, P. alni ssp. uniformis is apparently not damaging alder trees in Alaska. In Oregon it does cause limited root lesions on red alder. In Europe, surveys and modeling show that risk for infection is higher in warmer, slow moving waters, and in fine textured soil, especially clay loams. Although the disease is usually seen along river systems it has been found in sites well away from riverbanks or other water courses, for example in orchard shelter belts and in new woodland plantings. This suggests that the alder plants were already infected prior to planting. In Germany P. alni is disseminated on alder seedlings which became infected in the nursery. The alder pathogen was found in rootstocks of alders from three out of four commercial forest nurseries that were tested.

Forest and Wildland Hosts and Symptoms

In mid- to late summer diseased alders may exhibit leaves that are abnormally small, yellow and sparse, and which may fall prematurely, leaving the tree bare. Trees that have suffered from infection over several years show dieback, with dead twigs and branches. There may also be heavy production of cones, usually a sign of stress in an alder.

Although many trees die rapidly once the crown symptoms appear, in others the disease may take a chronic form with the loss of foliage and branch dieback increasing over time. In a single alder clump with several stems, one or more stems may be affected and even die, while other stems in the same cluster may recover or remain healthy.

Examination of the base of a tree with severe crown symptoms often reveals a tarry or rusty spot, sometimes occurring up to 3 meters from the ground. Beneath these bleeding spots the inner bark (phloem) is dead as a result of invasion by Phytophthora. When the inner bark is freshly exposed with a knife, the recently killed tissue is often mottled reddish to purple brown, and contrasts strongly with the creamy color of the adjacent healthy inner bark.

In Alaska, P. alni ssp. uniformis is occasionally isolated from riparian soil in alder thickets, but it has not been associated with disease. In Oregon, ssp. uniformis is one of several Phytophthora species causing limited necrotic lesions on alder roots.

The only trees described as affected in the wild are alder trees. P. alni is regarded as a serious threat to riparian woodland. Affected alder species include:

• Alnus cordata - Italian alder
• Alnus glutinosa - common alder (most susceptible)
• Alnus incana - grey alder (most resistant)
• Alnus viridis - green alder
• Alnus rubra - red alder (ssp. uniformis only)

Educational and Management Materials

• Phythophthora Disease of Alder