Introduction

In angiosperms the advent of flowering is accepted as a matter of course, and, in fact, the majority of these plants do produce flowers when internal and external conditions are favourable. Occasionally, however, one may notice a plant in which one or more flowers are deformed, or are in some way different from the remainder. In many cases the nature and causes of the deformity are not known, but there is one type which has been the subject of a considerable amount of work in recent years. In this, the floral axis, instead of producing normal sepals, petals and stamens, produces structures which bear some resemblance to ordinary leaves while the apex continues to grow instead of giving rise to the gynoecium. It would appear as if the plant had started the formation of a flower and then, when it was almost too late, changed instead to vegetative growth. Such a phenomenon is known as VEGETATIVE PROLIFERATION.

This type of abnormality has been observed in many plants representing most major trends of angiosperm evolution. The present author has noted it in plants as widely different as the garden Penstemon and the rush Juncus articulatus, as well as in a flowering peach and a number of sedge species. Other reports show that proliferation has been observed in roses, lupins and the native flax Phormium tenax. However, it is in the grass family that proliferation is most frequently found and it is in this group that the subject has been most thoroughly investigated.

The ultimate unit of a grass inflorescenice is the spikelet and it is necessary to understand the structure of this unit before looking into the nature and causes of proliferation in the group. A typical spikelet (Figs. 1 and 2) is a branch of determinate growth, bearing leafy bracts or glumes. The two lowermost glumes are usually sterile while each of the upper ones bears a flower in its axil. These fertile glumes are termed the lemmas. On the floral axis is first a prophyll or palea and then two small bracts the lodicules, these latter structures representing the reduced perianth. The stamens are attached above the lodicules, while the gynoecium occupies the apex of the flower. Thus the typical spikelet is composed of a number of flowers, together with their associated bracts or glumes, borne laterally on the spikelet axis.

In grasses the spikelets rather than the individual flowers proliferate and they do so in one of two ways. Firstly, the axis or rachilla may remain page 122 short and the sterile glumes unchanged, while the lemmas become successively more leaf-like from the base to the apex of the spikelet. The flowers in the axils of these leafy-lemmas are usually sterile and the rachilla apex develops into a normal stem apex giving rise to leaf primordia. Later an abcission layer forms above the sterile glumes and root primordia develop above this abcission layer, thus producing a bulbil capable of developing into a new plant when detached from the parent inflorescence. Such a type is illustrated in Figs. 3 and 4. Secondly, as in Fig. 5, the rachilla may elongate considerably above the unmodified sterile glumes. The lowermost lemmas are sterile while the uppermost produce normal flowers and fruit; there is a progressive shortening of the rachilla internodes from the base to the apex. This second type of proliferation does not result in the formation of a bulbil.

As is the case with most natural phenomena, many intermediate stages can be seen between the normal type of spikelet and either of the proliferation types, and although intergrades between the two proliferation types are not found, both of these can be observed on the same inflorescence. Despite their different appearance and structure, it is believed that both are effects of the same general cause.

When proliferation in grasses was first reported, its nature was not fully understood and the term vivipary was applied to it. This is an unfortunate use of a term which should be applied to the premature germination of seed which is still held by the parent plant, as is found in the mangrove Rhizophora. It is, however, an understandable error since the proliferating spikelet giving rise to a bulbil bears a striking resemblance to a spikelet containing germinating grains. Some authors overcome the difficulty by calling proliferation false vivipary, but this is unsatisfactory as it implies some connection with the viviparous habit. The most recent trend is towards the use of the term spikelet proliferation. However, the term vivipary will remain because races which regularly reproduce by the production of bulbils bear the varietal name vivipara, e.g. Poa alpina var. vivipara.

Spikelet proliferation has been recorded in some thirty grass species, including many of the important agricultural grasses. Some species regularly reproduce by the production of bulbils and these are referred to as the page break

PLATE I
Fig. 1 Side view of normal grass spikelet. Fig. 2: Diagrammatic longitudinal section of a normal grass spikelet. Fig. 3: Bulbil type of proliferation. Fig. 4: Longitudinal section through a bulbil showing progressive sterilisation of floral parts, development of a root primordium, the formation of the abcission layer and the vegetative apex. Fig. 5: Proliferation with elongated rachilla. AG = Abortive Gynoecium; AL = Abcission Layer; C = Lodicules; G = Gynoecium; L = Lemma; LL = Leafy Lemma; LP = Leaf Primordium; P = Palea; R = Rachilla; RP = Root Primordium; S = Stamen; SG = Sterile Glume; SL = Sterile Lemma; VA = Vegetative Apex.

page 124 VIVIPAROUS RACES, e.g. Poa alpina var. vivipara and Deschampsia alpina of the European artic-alpine areas. In these, proliferation is an hereditary character scarcely modified by the environment. Other species only occasionally produce proliferating spikelets and they are said to show EPHEMERAL PROLIFERATION. In the northern hemisphere many grasses are reported to have shown ephemeral proliferation while in New Zealand the following species are known to have produced bulbils and there are possibly many others: cocksfoot, Dactylis glomerata; crested dogstail, Cynosurus cristatus; timothy, Phleum pratense; and a native meadow grass, Poa lindsayi. These species show a greater tendency to proliferate than others and in cocksfoot it is almost a regular feature in late autumn.

Causes of Proliferation

In a high proportion of the grasses which have shown a tendency for proliferation the chromosome numbers are extremely variable. Some of the species concerned have developed a greater or lesser degree of polyploidy while others have developed chromosome numbers which are not direct multiples of the haploid number for the species and these are said to be ANEUPLOIDS. As an example, the species Deschampsia alpina has chromosome numbers of 26, 39, 41, 48, 52 and 56, with a basic haploid number of 13. A feature of aneuploid species is that they tend to be sterile, rarely producing fertile seed. Nygren (1949) in a survey on the relation between chromosome number and degree of proliferation developed in Deschampsia alpina, showed that the plant with a diploid number of 26 was perfectly normal and produced flowers which set ferile seed, while plants with numbers from 39-49 showed, with increasing chromosome number, an increasing tendency to proliferate. Thus with increasing sterility induced by the greater degree of aneuploidy, there is a greater tendency for plants to produce proliferating spikelets. In these circumstances natural selection would favour those plants which can reproduce their kind vegetatively.

The viviparous races are all highly aneuploid and are probably incapable of producing fertile seed. Proliferation in these is an hereditary character determined directly by the genotype and, because they always reproduce by this means, all members are genetically identical, or in other words they form a clone.

In those grasses which show ephemeral proliferation, control is not entirely genetical, the environment playing a large part in controlling the development of bulbils. In the majority of cases the proliferation is noted in the autumn when conditions are becoming cooler, the air is frequently more moist and the length of day is becoming shorter. It was first suggested that the damp conditions prevalent in autumn induced proliferation, but it has subsequently been shown that, although damp conditions are necessary for the establishment of the bulbils and hence those species which show a tendency to proliferate are found in regions where rainfall is plentiful, these conditions are not the actual cause of the proliferation. page 125 Opinion now is that ephemeral proliferation is induced primarily by a photoperiod unfavourable to flowering.

It is thus apparent that proliferation can be caused either by irregularity in the chromosome number of the species, or conditions unfavourable to flower production, and in most cases both of these causative factors are working together.

Discussion

In a recent article, Sussex (1956) has reviewed the causes of flowering in angiosperms, and it was shown that the length of day is one of the characters of prime importance in determining whether a plant will flower or not. Brief mention was made of the necessity, in many cases, for the exposure of germinating seed or young plants to the effect of cold temperatures. Many plants which flower only when the length of day is above a certain minimum and are hence classified as long-day plants, will not flower, even when exposed to the correct photoperiod, unless they have been subjected to a period of cold temperatures. This pretreatment is known as VERNALISATION. Exposure of plants to cold temperatures during germination or early growth was first thought to be the only way of vernalisation, but then in a few species it was found that if young plants were grown in short-day conditions they would react as if they had been exposed to low temperatures. Thus in these species, vernalisation can be given in the form of low temperatures or short days and in natural winter conditions both are given together. The exposure of plants to suitable periods of vernalisation followed by adequate daylengths is believed to promote the formation of a hormone, as yet not isolated, which induces firstly the formation of the flowering branch or, in grasses, the culm and later the formation of the flowers. Although the nature of this flower-promoting hormone is not known it is conveniently called FLORIGEN.

Most grasses which show ephemeral proliferation are from temperate or cool-temperate regions where they receive a period of vernalising conditions in the winter followed by long photoperiods in the summer. Thus they can be classified as long-day plants.

In the most recent work on proliferation (Wycherley, 1954) two possibilities have been presented to account for the production of vegetative spikelets.

Firstly, that the critical concentration of florigen for culm initiation is the same as for flower initiation but, as inflorescence development proceeds, the hormone may be used up so that at the time of flower initiation the concentration of florigen is below the required minimum and the spikelets proliferate.

Secondly, that the critical concentration of florigen necessary to induce culms may be lower than that required to induce flowers and if the concentration of florigen at culm initiation is at the minimum then there will not be enough for flower initiation and the spikelets will proliferate.

The second postulation is the one most favoured. It is suggested that in plants showing ephemeral proliferation, the concentration of the flowering hormone necessary for culm and flower formation may be nearly the same and hence rarely will there be insufficient to complete the formation of flowers. However, by the end of the growing season most of the florigen will have been used up in the formation of earlier culms and inflorescences and no more will be produced because of the unfavourable photoperiod. Thus in these plants proliferation is most prevalent in the autumn when the concentration of florigen will be at a minimum for culm initiation and insufficient for flower initiation. In the viviparous races, on the other hand, the critical level of florigen for flower initiation may be so much higher than that for culm development that the plants always proliferate.

In both these races, i.e. those showing ephemeral proliferation and the viviparous races, the character of proliferation is genetically controlled, in that the genotype determines at what concentration of florigen the processes of culm and flower initiation will take place. In the former it is indirect control, as the concentrations of florigen necessary for culm and flower initiation are almost the same, the environment controlling the level of florigen in the plant, while in the latter it is direct control.

These explanations are purely hypothetical but until the nature of the flowering stimulus is more fully known little further progress can be made. From these observations on proliferation it would appear, however, that flowering is not an all-or-nothing phenomenon as has been postulated previously.

Acknowledgements

Thanks are expressed to Professor W. R. Philipson of the University of Canterbury, under whose guidance the groundwork of this topic was studied. Also to Dr. P. R. Wycherley of the Rubber Research Institute, Malaya, and Mr. W. A. Jacques of Massey Agricultural College, for the loan of literature and material.