Fasciation

Binggeli, P. (1990) Occurrence and causes of fasciation. Cecidology 5, 57-62.

There has recently been a renewed interest in the study of fasciation (see Cecidology Vol.5 No. 1), and the cause of fasciation is now the subject of some debate. In this paper I want briefly to review the subject and to supply an up-to-date reference list which will give interested readers access to a large and slightly obscure literature. I also include some unpublished information on the occurrence of fasciation in sycamore (Acer pseudoplatanus L.).

Fasciation in the Plant World

The word fasciation comes from the Latin fascia, meaning a band. The phenomenon has been widely observed in the plant world, and various aspects of our knowledge of fasciation have been thoroughly reviewed by White (1948) and Gorter (1965). Fasciation can affect the whole plant or any of its component parts. In true fasciations the growing point is generally ridge-like instead of circular, leading to a flat ribbon-shaped structure, although there is another much rarer type, characterised by a ring-shaped growing point, which produces a hollow shoot. Fasciation has been recorded in 107 plant families and is common in the Rosaceae, Leguminosae, Onagraceae, Compositae, and Cactaceae. It is especially prevalent in species with indeterminate growth patterns - i.e. those that do not conform to any fixed pattern of growth.

Fasciation is only one of the numerous variations, often exhibited in the form of completely abnormal structures, which may be observed in plants. Such abnormal forms of organs were widely studied during the 19th Century and the early part of the 20th Century and the subject was known as teratology (the science of wonders or monsters). Wordsell (1915, 1916) surveyed the teratological features of plants and Heslop-Harrison (1952) reassessed the biological theories underlying such phenomena. Meyer (1966) and Meyerowitz et al. (1989) provide more recent treatments of floral abnormalities.

Fasciation in Sycamore

Most trees and shrubs, both coniferous and broad-leaved, can bear fasciated branches (see, for example, Tanner 1930 and Rance et al. 1982), and these are easily observed on deciduous trees in winter. Some species, including the sycamore, are far more susceptible than others to malformations. Sycamore is a very variable species and variations in the number of plant parts, such as carpels and cotyledons (Binggeli & Rushton 1983), and in the sex of flowers and inflorescences (Binggeli 1990) have often been recorded. Likewise, fasciation is also common in the sycamore, including fasciation of branches, twigs, petioles, inflorescences, and flowers.

Young sycamores have short and long shoots, while mature trees have only short shoots. The short shoots of juveniles are borne on the side of the main branch axis and usually grow about 5cm per year: some are fasciated, with a ridge rarely exceeding 0.5cm in width. On the long shoots (usually the leading stem or the main axis of a branch) growth reaches up to 1m per year. At its widest, the fasciation is about 5cm wide and curved, and usually branches into several shoots. At this point the arrangement of leaves, buds and twigs does not show any distinct pattern, but by looking at the longest shoots it is possible to see a change in the position and the number of leaves and buds along the length of the stem. Buds occur at the base of the leaf petiole and, like the leaves, normally occur in whorls of two. In some cases it may be observed that just above the bud scar the leaf and bud number per whorl increases from two to three and then to four: the shoot later becomes fasciated and all apparent order in leaf and bud position is lost. In sycamore it appears that the increase in the number of parts eventually leads to the production of fasciation. This suggest that there is a lack of hormonal control in the growing point and, as the trait appears to be more come in some areas than other, that the environment strongly affects its expression.

Causes of Fasciation

The following list of causes of fasciation is based on Gorter (1965) unless otherwise stated. More recent work on the causes of fasciation include Albertsen et al. (1983), Bairathi & Nathawai (1978), Behera & Patnaik (1982), Driss-Ecole (1981), LaMotte et al. (1988) and Rance et al. (1982), together with the references therein.

1) Genetic Fasciation

Fasciation of the stems of the 'mummy pea' was one of the original seven Mendelian pairs of characters. This character is often controlled in plants by a single recessive gene, but inheritance can also be non-Mendelian. Many species, including vegetables such as the Swiss chard, exhibit true-breeding fasciated lines, although the expression of the character is very dependent on environmental conditions - especially temperature and nutrition. Because the gene conditioning fasciation exhibits incomplete penetrance, the character may assume any of many degrees of expression.

2) Physiological Fasciation

A) Natural Environmental Factors

a) Attack by Insects Several insect species have been found to produce fasciation. Band and ring fasciation in Oenothera spp. are caused by the presence of eggs of the genus Mompha in the growing point (Knox 1908). A stem of common hawkweed (Hieracium vulgatum) attacked by the gall was Aylax [= Aulacidae] hieracii was normal below the gall but fasciated above it (Hus 1908). Fasciation of the fleabane (Conyza canadensis) is caused by Cecidomyia erigeroni. This gall midge lays its eggs on the surface of the plant and the resulting larvae penetrate the tissues (Hus 1908). On wild radish (Raphanus raphanistrum), Molliard (1900) found the tunnel of a beetle larva running through the centre of every fasciated shoot and extending upwards to the growing point. He made similar observation on hawkweed oxtongue (Picris hieracoides), where he found lepidoptera larvae in a gallery situated in the central part of the growing point. According to Peyritsch (1888) the mite Phytopus is the possible cause of fasciation in the Valerianaceae. Munci & Patel (1930) showed that the mealybug (Pseudococcus spp) that infest sweet peas along with fungi and bacteria are not the cause of the observed fasciation, and their work demonstrates that field observations alone are insufficient to ascertain the causal agent of fasciation.

b) Pressure Underground shoots that pierce the ground, such as asparagus, tend to become fasciated.

c) Seasonal Influences Time of sowing may influence the degree of fasciation, with earlier sowing appearing to produce larger numbers of fasciated plants. Crowding has often been reported to produce a decrease in the percentage of fasciated plants.

d) Temperature Low temperature followed by high temperature causes fasciation in Hyacinthus and may be a cause of fasciation in other plants.

e) Mineral Deficiency Zinc deficiency is known to cause fasciation (Rance et al. 1982).

B) Artificially Applied Factors 

a) Decapitation of Seedlings and Defoliation Amputation of the main stem of seedlings induces fasciation in several species. Defoliation produces a similar reaction. Blaringhem (1907) reported that heavy pruning induced fasciation in deciduous trees. 

b) Wounding of the Growing Point Wounding causes fasciation as well as all kinds of abnormalities. 

c) Ionizing Radiation (X-rays and gamma-rays). 

d) Infection with Fungi, Bacteria, and Viruses 

e) Polyploidizing Agents (colchicine, morphine, phenyl-urethane, etc). 

f) Nutrition Good nutrition, including high rates of manuring, increases the occurrence of fasciation.

g) Water Shortage Plants with indeterminate inflorescences when kept under drought conditions prior to flowering and then subjected to heavy watering and high nutrient levels will produce numerous fasciations (Hus 1908). h) Application of Growth Regulators TIBA (2,3,5-triodobenzoic acid), for example, induces fasciation, particularly ring fasciation, and many other abnormalities, including distortions and fusion of organs. (See also Astié 1963). 

i) Photoperiod Fasciation may be induced by increasing or decreasing the photoperiod - the lenght of day experienced by the plants (Astié 1963).

Conclusions

Fasciation can be caused by a variety of natural and artificial agents. From the literature, it appears that few cases of fasciation have been shown to be caused by insects, although most reports of fasciated plants contain no information as to what may have induced the fasciation. Information is clearly needed in order to find out the relative importance of the above-listed agents. To determine the causes of fasciation in a particular plant species requires a good deal of experimental work, as has been shown by Muncie & Patel (1930).

Acknowledgement

Brain S. Rushton's comments and corrections are much appreciated.

References

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Astié, M. (1963) Tératologie spontanée et expérimentale. Ann. Sci. Nat., Sér. 12, 3, 619-844.

Bairathi, M.K. & Nathwai, G.S. (1978) Morphology and anatomy of fasciated plants of Sannhemp. Flora 167, 147-157.

Behera, N.C. & Patnaik, S.N. (1982) Histology of mutants in Amaranthus hypochondriacus. Indian J. Genet. Plant Breed. 42, 5-10.

Binggeli, P. (1990) Detection of protandry and protogeny in sycamore (Acer pseudoplatanus L.) from infructescences. Watsonia 18, 17-20.

Binggeli, P. & Rushton, B.S. (1983) Schizocarpic variation in sycamore (Acer pseudoplatanus L.) in Ireland. Ir. Nat. J. 21, 120-125.

Blaringhem, L. (1907) Mutation et traumatismes. Alcan, Paris.

Driss-Ecole, D. (1981) Fasciation from excised shoot apices in Celosia cristata (Amaranthaceae) cultivated in vitro. Can. J. Bot. 59, 1367-1373.

Gorter, C.J. (1965) Origin of fasciation. In Rhuland, W. (Ed.) Encyclopedia of Plant Physiology, Vol. 15(2), 330-351. Springer Verlag, New York.

Heslop-Harrison, J. (1952) A reconsideration of plant teratology. Phyton 4, 19-34.

Hus, H. (1906) Fasciation in Oxalis crenata and experimental production of fasciations. Rep. Missouri bot. Gard. 17, 147-152.

Knox, A.D. (1908) The induction, development and heritability of fasciation. Publ. Carnegie Inst. (Wash.) No. 98, 3-21.

LaMotte, C.E., Curry, T.M., Palmer, R.G. & Albertsen, M.C. (1988) Developmental anatomy and morphology of fasciation in the soybean (Glycine max). Bot. Gaz. 149, 398-407.

Meyer, V. (1966) Flower abnormalities. Bot. Rev. 32, 165-195.

Meyerowitz, E.M., Smyth, D.R. & Bowman, J.L. (1989) Abnormal flowers and pattern formation in floral development. Development 106, 209-217.

Molliard, M. (1900) Cas de virescence et de fasciation d'origine parasitaire. Rev. gen. Bot. 12, 323-328.

Muncie, J.H. & Patel, M.K. (1930) Fasciation of sweet peas. Am. J. Bot. 17, 218-230.

Peyritsch, J. (1888) Uber kunstliche Erzeugung von gefullten Bluthen und andere Bildungsabweichungen. S. B. kais. Akad. Wiss. Wien, Math. nat. Kl. 97, 597-605.

Rance, S.J., Cameron, D.M. & Williams, E.R. (1982) Correction of crown disorders of Pinus caribaea var. hondurensis by application of zinc. Pl. Soil 65, 293-296.

Tanner, H. (1930) Uber Verbänderungen (Fasciationen) an unseren Waldbaumen. Jahrb. St. Gall. Naturw. Ges. 65, 47-70.

White, O.E. (1948) Fasciation. Bot. Rev. 14, 319-358.

Worsdell, W.C. (1915) The principles of plant teratology. Vol. I. Ray Society, London.

Worsdell, W.C. (1916) The principles of plant teratology. Vol. II. Ray Society, London.

Updated Bibliography

Cooper, J.I. (1993) Virus diseases of trees and shrubs. Chapman & Hall, London.

Juvik, J.O. & Juvik, S.P. (1992) Mullein (Verbascum thapsus): the spread and adaptation of a temperate weed in the montane tropics. In Stone, C.P., Smith, C.W. & Tunison, J.T. (Eds) Alien plant invasions in native ecosystems of Hawai'i: management and research, pp. 254-270. University of Hawaii Press, Honolulu.

Kulkarni, D.K., Kumbhojkar, M.S. & Phatak, M.S. (1991) Fasciated inflorescence axis of Cassia fistula L. Biovigyanam 17, 51-54.

Rösler, D. & Rösler, R. (1998) Neuigkeiten zur teratologie der Eibe (Taxus baccata L.). J. for. Suisse 149, 405-410.

Saxena, S.K. & Tripathi, J.P. (1990) Teratological observations in inflorescence axis of Cassia fistula Linn. Ind. Forester 116, 245-247.

Seehann, G., Schultz-Dewitz, G. & Wenk, M. (1994) Abnorme holzstrukturen. Teil 3: Verbänderungen an Spitzentrieben von Coniferen. Drevarsky Vyskum 39, 9-20.

Tang, Y. & Knap, H.T. (1998) Fasciation mutation enhances merismatic activity and alters pattern formation in soybean. Int. J. Pl. Sci. 149, 275-282.

Tang, Y. & Skorupska, H.T. (1997) Expression of fasciation mutation in apical meristems of soybean, Glycine max (Leguminosae). Am. J. Bot. 84, 328-335.