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Volume 82, 1954-55
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The Genus Albugo in New Zealand

[Read before the Auckland Institute. April 28. 1954; received by Editor, May 7. 1954.]

Abstract

The fungus genus Albugo is described, and its validity is upheld against Cryslopus, Lev. and Cyslopus de Bary. Four species, A. crucifeiutum, A mcsembryanthemi, A. quad-rata and A. tragopogi are found in New Zealand, all being host family specific. A mesembryanthemi is described as a new species.

Albugo is a clearly defined cosmopolitan genus belonging to the order Perono-sporales of the Phycomycetes. Species are commonly known as “white rusts” because of the superficial resemblance of their conidial postules to rust sori. The genus is strictly parasitic in habit and host family specific. Clavate conidiophores bearing conidia in chains are closely packed in a subepidermal sorus. Sexual organs are borne terminally or laterally on mycehal hypliae within the host tissue. Oospores are dark-coloured, with sculptured walls.

Persoon (1801) included Albugo as a section of the genus Uredo, characterised by possessing white spores. Recognising its affinities with the Phycomycetes Gray (1821) defined Albugo as a separate genus containing three species, A. cruciferarum, A. tragopogi and A. petroselini. The group was not mentioned by Pries in Systema mycologicum 1821–32. Leveille did not recognise Albugo and erected a new genus Cystopus in 1847. Oospores and sex organs were not described until de Bary in 1865 revised the genus to include the perfect stage. Kuntze in Revisio genera plantarum 1891 correctly revived the name Albugo.

Ramsbottom (1916) and Wakefield (1927) when reviewing the genus recognised Cystopus de Bary since de Bary was the first to describe the perfect stage. According to the alteration in Article 57 of the International Code of Botanical Nomenclature made at the Seventh International Botanical Congress, Stockholm. 1950, this distinction is no longer applicable to the Phycomycetes and the genus Albugo must therefore be conserved against Cystopus de Bary.

Again Article 20(f) of the revised code stated that “Volume I of the Systema is treated as having appeared January 1, 1821”. The purpose of this rule is that “fungus binomials set up by S. F. Gray, Schweinitz, Persoon and others in the period between January 1, 1821, and December 31, 1832, may be legitimate if not so included by Fries.” (Stevenson & Rogers, 1950). Therefore Albugo must replace Cystopus Lev.

In conserving this genus, one species described by Gray has to be taken as type, Albugo crucirifraum being selected since it is widespread rind was also regarded as the type of Cystopus under the name of Cystopus candidus Pers. ex Lev.

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I wish to thank Dr. G. H. Cunningham and Miss Joan M. Dingley for help in preparation of the manuscript and Miss Beryl Hooton for Latin description of one species.

Albugo (Pers.) S. F. Gray, A Natural Arrangement of British Plants, 2, 540, 1821.

  • 1801. Uredo Albugo Pers. Syn. Meth. Fung. 223.

  • 1833. Erysibe sensu Wallr. Flora Crypt. germ. 2. 193 (pro parte).

  • 1847. Cystopus Lev., Ann. Sci. Nat. IV, 8, 371.

  • 1863. Cystopus de Bary, Ann. Sci. Nat. IV, 20, 31.

Parasitic and host family specific. Mycelium intercellular, widespread, particularly in leaves, bearing simple globose intracellular haustoria. Conidial sori subepidermal, later erumpent, forming white to cream mealy patches on all aerial parts of the host. Conidiophores crowded, clavate, hyaline, forming basi-petal chains of conidia joined by colourless connective links. Conidia all alike or the terminal conidium larger than the others, sterile; globose, elliptical, oblong, cubical or truncated obovate, hyaline; Mall smooth, equally thickened throughout or with an annular thickened band. Sexual organs: antheridia and oogonia borne singly on short terminal or lateral mycelial branches within the host tissue; oogonia globose, differentiated into periplasm and oosphere; antheridia small, club-shaped, arising near the oogonia. Oospores thick-walled, globose; epispore dark-coloured, ornamented with warts, ridges or reticulations. Germination by zoospores.

Type Species. Albuyo cruciferarum S. F. Gray.

Distribution. World-wide.

Key TO Species

Conidial wall with annular thickened band 1. A. tragopogn S. F Gray
Conidial will without annular thickened band Oospore wall with waits or short branched ridges 2. A. cruciferarum S. F. Gray
Oospore wall reticulate
Spine present in areolae of reticulations 3. A. quadrata (Wallroth) Baker
Spine absent from areolae of reticulations 4. A. mesembryanthemr Baker
  • 1. Albugo tragopogi S. F. Gray, A Natural Arrangement of British Plants, 2, 540, 1821. (Fig. 2)

  • 1801. Uredo Candida b. tragopogi Pers. Syn. Meth. Funy. 223.

  • 1810. Uredo cubica Strauss, Ann. Well. Gcs. f. naturk, 2, 86.

  • 1815. Uredo tragopogi DC., Flore Fiance, 2, 237.

  • 1862. Cystopus, spmulosus de Bary, Rabenh. Fung. Evr., No. 479.

  • 1863. Cystopus cubicus de Bary, Ann. Sci. Nat. IV, 20, 132.

  • 1886. Cystopus tragopogonrs Schroet., Krypt. Fl. Schles. 3, i, 234.

  • 1891. Albugo spinulosa Kuntze, Rev. Gen. Pl. 6, 658.

Conidial sori erumpent, mainly on the lower surface of leaves, forming small scattered irregular ivory-white pustules. Hyphae 4–6μ. diameter, much branched, hyaline, thin-walled; intracellular haustoria simple. Conidiophores subclavate, hyaline, 20–48 × 12–24μ, average 30 × 19μ. Conidia joined by colourless connecting inks into chains; terminal conidia pallid yellow, 20–32μ. diameter, average 24μ., wall 4μ, equally thickened; other conidia hyaline to pallid yellow, thin-walled except for a distinct annular thickened band 3–4μ thick, cubical to oblong, 17–30 × 14—28μ, average 21 × 19μ. Oospores dark brown to black, globose, 40–72μ diameter, average 53μ.; epispore 4–5μ. thick, closely reticulated with areolae 3–4μ. wide; reticulations 0·5–2·2μ high,

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Type Locality. Europe.

Distribution. World-wide.

Habitat. On Compositae.

Brachycome sinclairii Hook. f. Canterbury. Castle Hill, 1.500ft., January, 1928; G. H. Cunningham.

Cirsium arvense (L.) Scop. Auckland. Tauranga, January, 1924; J. C. Neill-G. H. Cunningham.

Cotula australis Hook., f. Wellington. Upper Hutt, May, 1953; A J. Healy.

Craspedia uniflora Forst. Canterbury. Mt. Torlesse, 2,000ft, January, 1928; G. H. Cunningham.

Lagenophora petiolala Hook. f. Canterbury. Black Birch Creek, Hermitage, January, 1928; G. H. Cunningham.

Senecio scorzoneraides Hook. f. Westland. Mt. Rangitaipo, 3,500ft., February, 1928; G. H. Cunningham.

Soliva valdivtana Ph Wellington. Upper Hutt, May, 1953, A. J. Healy.

Tragopogon porrifolius L. Auckland. Auckland City, December, 1947; unknown collector.

Though A. tragopoyi is recorded from four New Zealand endemic plants, Brachycome sinclairii, Craspedia uniflora, Lagenophora petiolata and Senecio scorzoneroides it is uncommon in the Dominion.

Picture icon

1.—Oospore of Albugo quadrata.
2.—Oospore of A tragopogi.
3.—Oospoie of A. cruciferarum.
4.—Oospore of A mesembryanthemi.

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The species is differentiated from others present in New Zealand by the presence of an annular thickened band on the conidial wall and by the finely reticulated ootpore wall. Antheridia and oogonia were not present in material examinee.

2. Albugo cruciferarum S. F. Gray, A Natural Arrangement of British Plants, 2, 540, 1821. (Fig. 3)

  • 1791. Accidium candidum Pers Gmcl. Sysl. Nat. 2, 1473.

  • 1801 Uredo Candida Pers., Syn Meth Fung. 223.

  • 1847. “Cyslopus candidus” Lev., Ann. Sci. Nat. Ill, 8, 371.

  • 1863. Cystopus candidus de Bary. Ann.Set Nal. IV, 20, 31.

  • 1891. Albugo Candida (Pers.) Kuntze, Rev. Gen. Plant. 2, 638.

Conidial sori formed on all aerial parts of the host, often causing distortion of tissues, in small scattered or gregarious patches or covering almost the entire surface of the host, erumpent, white to cream in colour Mycelial hyphae sparse, 4–12μ. diameter, hyaline, thin wailed, bearing simple intracellular haustoria. Conidiophores crowded into son, clavate, hyaline, 14–44 × 8–18μ, average 28 × 13μ. Conidia joined by colourless connectives into chains, all alike, hyaline, globose. elliptical or truncated obovate, thin walled, without annular thickened band, 12–23 × 12–20μ, average 17 × 16μ. Sex organs infrequent, in tissues or stein and capsule, oogonia borne singly on short terminal or lateral branches, globose, about 40μ, diameter; antheridia club-shaped. 16–24 × 24–32μ, arising near the oogonia; oospores globose, dark brown, 40–60μ, average 50μ.; epispore 4–7μ thcick, tuberculatc with flattened branched ridges.

Type Locality. Europe.

Distribution. World-wide.

Habitat. On Cruciferac.

Brassica campestris L. Auckland Mt Eden, September, 1953; S. D. B. Mt. Albert, August. 1953; J. M. Dingley.

Brassica oleracea L var. bolrytis L. Auckland. Mt. Albert, March, 1946; J. D. Atkinson.

Brassica rapa L. Wellington. Levin, September, 1919; G. H. Cunningham. Weraroa September, 1919; W. Standring.

Capsella bursa-pastoris (L) Medik Auckland Ellerslie, June, 1953; S. U. B. Tamaki June, 1953, R. F. de Berg. Wellington. Weraroa, July 1919; G. H. Cunningham. Wairarapa. February, 1953; A. J. Healy. Upper Hutt, April, 1953; A. J. Healy. Wadestown. December, 1953; J. M. Dingley Canterbury. Ashburton, January, 1925: J. C. Neill. Christchurch, November, 1946; R. Grainger. Otago. Ettrick. October, 1924; J. C. Neill.

Cardamine sp. Wellington. Upper Hutt, December, 1953; A. J. Healy.

Cardamine hirsuta L. Auckland Remuera. September, 1943; J. M. Dingley Mt Albert, August. 1953; J. M. Dingley. Wellington. Hutt Valley, December. 1953, A J. Healy.

Cleome spinosa L. Auckland. City, March. 1952; M. Arken Hawke's Bay. Gisborne. February, 1951; J. D. Kennedy.

Lepidium oleraceum Forst Auckland. Little Barrier Is., October, 1945; J. M. Dingle.

Lepidium ruderale L. Wellington. Wairarapa. February, 1953; A. J. Healy. Trentham, March, 1953; A. J. Healy.

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Lepidium sativum L. Wellington. City, November, 1880; T. Kirk.

Malcomia mantima R. Br. Auckland. Remuera, July, 1930; T. A. Hunter. Epsom, August, 1953; J. M. Dingley.

Raphanus sativus L. Auckland. Mt. Albert, (October, 1945, N. Wright Orakei, January, 1946, D. W. McKeuzie. Mt. Albert, September, 1953; J. M. Dingley. Three Kings, March, 1954; S. D. B.

Rorippa islandica (Oeder) Borbas Wellington. Hutt Valley, February, 1953, A, J. Healy.

Sisymbrium officinale (L.) Scop. Auckland. Mt. Albert, September, 1953. J. M. Dingley Mt. Eden, September, 1953; S. D. B. Wellington. Hutt. Valley, February, 1953; A. J. Healy.

Persoon's epithet “Candida” has been universally applied to this species. Leveille, however, did not use “Candida” until 1847, and as there is no rule for conserving a specific epithet, “cruciferarum” must be employed in its stead.

Since Colenso (1886) first recorded the cosmopolitan Albugo cruciferaum in New Zealand, it has been found on many cruciferous hosts. Many overseas workers (Hiura, 1930; Napper, 1933; Togashi and Shibasaki, 1934) have shown by cross inoculation experiments the existence of numerous biological races within the species which are confined to various sections of the Cruciferae.

Apart from Lepidium oleraceum Forst, an endemic species, all hosts are introduced. Clcome spinosa L., a member of the Capparidaceae (closely allied to the Cruciferae) is commonly a host for Albugo cruciferarum. The fungus is morphologically indistinguishable from that on Cruciferae.

3. Albugo quadrata (Wallr.) n. comb. (non. Kalchbr & Cke., Grevillea, 9, 22, 1880). (Fig. 1)

  • 1815. Uredo portulacae DC. Flore France, 5. 88.

  • 1833. Erysibe quadrata Wallr.. Fl. orypt germ. 2. 194.

  • 1847. “Crystopus porlulacae” Lev., Ann. Sci. Nat. III, 8, 371.

  • 1863. Cystopus portulacae de Bary, Ann. Sci. Nat. IV, 20, 30. 130.

  • 1891. Albugo portulacae (DC.) Kuntze, Rev. Gen. Pl. 2, 658.

Conidial sori erumpentforming scattered irregular cream pustules on leaves and stems. Hyphae frequent below pustules, thin walled, hyaline. average 6μ. diameter; intracellular haustoria simple Conidiophores crowded into sori. subclavate, hyaline. 32–44 × 12–20μ, average 37 × 15μ. Conidia borne in chains with colourless connecting links terminal conidia yellowish, thick walled. 1 5–2 5μ, with a basal peg-like invagmation of the cell wall; other conidia hyaline, [ unclear: ] thin-walled, without annular thickening, elliptical to oblong, 16–22 × 12–18μ. average. 19 × 15μ. Oospores borne in the tissue of the leaf underneath pustules, dark brown to black, subglobase. 36–56μ diameter, average 48μ, wall 6μ thick; epispore reticulated, with a coarse spine about 4μ high in each areola.

Type Locality. France.

Distribution. World-wide.

Habitat. Portulaca oleracca L. Auckland. Mt Albert, February, 1945; G. H. Cunningham. Mt. Albert. February, 1951, J. M. Dingley. Mt. Albert, February, 1954; S. D. B.

Wallroth in 1833 neglected to recognise Uredo portulacae of de Candolle and renamed the species Erysibe quadrata. It was not until 1847 that Leveille re-applied the epithet “portulacae” According to the revised code, nomenclature

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of this group is taken as starting from January 1, 1821, and therefore Wallroth's epithet “quadrata” should be employed on the grounds of priority.

Kalctbrenner and Cooke in 1880 named a new species found on Hypoestes verticillata in South Africa, Cystopus quadratus. However, Wallroth's epithet “quadrata” has priority and should be conserved.

Throughout the world Albugo quadrata is confined to the one host Portulaca oleracea.

4. Albugo mesembryanthemi n.sp. (Fig. 4)

Sori conidii in foliis et calice, albi vel cremer virides, sieei aurantio-brunner, inaequaliter rotundae maculae ad 3 mm. diam. in exsiccatis depressae Hyphae parietibus tenuibus ad 12μ diam, haustoriis simplicibus intra cellulas. Conidiophora in soris congregata, cylindrata, 45–90 × 12–18μ. (67 × 19μ. med.), eonidia continua ferentia. Conidia dualia, terminate leviter maius 28–32μ., pallide luteum, pariete crasso, altera hyalina, parietibus tenuibus nullis annulis densatis, vinculis pellucidis conjuncta, cubica, globosa vel elliptica, 16–28 × 12–28μ (22 × 19μ. med). Oospora: fusco-brunneae vel nigrae, 50–76 × 44–76μ (61 × 60μ. med.) pariete 4—6μ crasso, episporiis reticulatis, areolis 4–6μ. latis.

Comdial sori on leaves and calyx, white to cream when fresh, turning orange brown then dry, forming irregularly circular spots up to 3 mm. diameter, becoming sunnken in dried specimens. Hyphae thin-walled, to 12μ diameter; haustoria intracellular, simple Conidiophores crowded into son, cylindrical, 45–90 by 12–18μ, average 67 × 19μ, bearing conidia in chains Conidia of two types: terminal conidium slightly larger, 28–32μ thick-walled and pallid yellow; other conidia dyaline, thin-walled without annular thickened band, joined by colourless connecting links, cubical, globose or elliptical, 16–28 × 12–28μ., average 22 × 19μ Oospores dark brown to black, 50–76 × 44–76μ., average 61 × 60μ., wall 4–4μ. thick; epispore reticulated, areolae 4—6μ wide.

Distribution. New Zealand.

Habitat. On Mesembryanthemum spp.

Mesembryanthemum oustrale Sol. Auckland. Piha. August, 1953, J. M. Dingley; type collection, P. D. D. herb. No. 12350.

Mesembryanthcmum spp. cult. Auckland. Tauranga, October, 1945; J. Hume Remnera, May, 1953; J. M. Dingley. Orewa, June, 3953; S. D. B. Wellington City. January, 1921, G. H. Cunningham. Canterbury. Christchurch, January, 1953; L. Hurndell.

Although A. mesembrayanihem has been found on the endemic Mesembry-anthemum australe Sol, it is not common on this host. Cultivated Mesembry-anthemums, which are natives of South Africa are, however, severely attacked in New Zealand There do not appear to be any overseas records of an Albugo species parasitising this genus.

Albugo guadrata differs in possessing smaller conidiophores and a reticulated oospore wall with coarse spines. The South African A. ausfro-africana Syd. which parasitises Aizoon rigidum, a member of the Aizoaceae, has a papillate oospore wall.

No antheridia or oogonia are present in the material examined.

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Literature Cited

Colenso, W., 1886 Trans. N.Z. Institute, 19, 301–313.

Gray, S. F., 1821 A Natural Arrangement of British Plants. 1. 824 pp., 2. 757 pp.

Hiura, M., 1930. Jap. Jour. Bot. 5. 1–20.

Napper, Maude E., 1933. Jour. Pomol. & Hort. Science, 2, 81–100.

Persoon, C. H., 1801. Synopsis Methodica Funqorum. Pars I and II. 706 pp.

Ramsbottom, J., 1916. Jour. Bot, 54, 77.

Rogers, D. P., 1949. Farlowia, 3, 425–493.

Stevenson, J. A., Rogers, D. P., 1950. Plant Disease Repoter 34. No. 11. 327–333

Togashi, K., Shibasaki, Y., 1934. Bull. Imper. Coll. Agric. & Forestry. 18, 88 pp.

Wakefield, E. M., 1927. Bothalia, 2, lb, 242–246.

Wilson, G. W., 1907. Bull. Toney Bot. Club, 34, 61–84.