ENVIRONMENTAL CONTROL OF CLEISTOGAMY IN PRAIRIE GRASS {BROMUS UNIOLOIDES H.B.K.)
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1 ENVIRONMENTAL CONTROL OF CLEISTOGAMY IN PRAIRIE GRASS {BROMUS UNIOLOIDES H.B.K.) BY R. H. M. LANGER AND D. WILSON* Lincoln College, Canterbury, New Zealand [Received 2 May 1964) SUMMARY In long days (16 hours) flowers of prairie grass {Bromus unioloides H.B.K.) were almost invariably cleistogamous. In shorter photoperiods chasmogamous flowers were the rule provided soil moisture was high. Chasmogamy was attended by greater anther length but later anthesis than occurred in the cleistogamic condition. Filaments and lodicules were small in cleistogamous flowers and autogamous pollination occurred soon after emergence from the leaf sheath. INTRODUCTION Prairie or rescue grass forms part of a complex of American species whose taxonomy has not been fully clarified. The name Bromus unioloides H.B.K. was widely accepted until Hitchcock (1934) proposed that it be changed to B. catharticus Vahl., although Hubbard (1956) contended that the earlier name be retained. More recently. Raven (i96) has argued that B. tvilldenovii is the correct name for prairie grass, while a second species, B. unioloides {B. haenkeamis) can be distinguished from it on account of its different habit and ecological preferences. To ensure continuity with earlier literature, and pending further clarification of the taxonomic problems, we propose to use the name B. unioloides H.B.K. here. Facultative cleistogamy has previously been described in members of the genus Bromus. Harlan (1945) has reported that B. carinatus produces abundant chasmogamous flowers in the spring but that unfavourable conditions cause later flowers to become cleistogamous in varying degrees, depending on the strain. It was possible for both types of flower to appear on the same panicle. In B. unioloides chasmogamy has also been shown to occur early in spring, to be followed by the production of cleistogamous flowers in the summer (Ragonese and Marco, 1941). Further investigation of this seasonal pattern indicated that the latter were formed in photoperiods exceeding 14 hours, while hours of light per day resulted in chasmogamy. However, length of day did not appear to be the sole controlling factor, for, although extending the day in winter caused cleistogamous flowers to be produced, reducing the day in summer failed to yield the expected chasmogamous plants. Differences in light intensity did not appear to be involved, but possible variations in temperature and water supply were not investigated (Ragonese and Marco, 1943). More recently Brown (1952) has in fact shown that in Stipa leucotricha the cleistogamic condition can be induced by reduction in soil moisture. This suggested the necessity for further work on prairie grass, particularly as control over the type of flower formed is important in relation to any breeding programme with this grass. The anthers of chasmogamous flowers are large and are extruded, thus facilitating emasculation, whereas self-pollination occurs in cleistogamic flowers. * Present address: Grasslands Division, D.S.I.R., Palmerston North. 8
2 Photoperiodism and cleistogamy in Bromus METHODS Three experiments were performed, the first to test the effect of day length and temperature, the second to study the role of soil moisture, and the third to compare the rate of anther growth in the two types of flower. Experiment i Plants of a commercial line of prairie grass were grown singly from seed in soil and were maintained in an 8-hour day for the first 2 months, during which time they remained vegetative. Groups of twenty-five randomly selected plants were then placed in photoperiods of 1.5 or 16 hours either in a heated glasshouse, or outside. All plants received 8 hours of natural illumination followed by the required period of artificial light from 15 watt mercury incandescent lamps. In the autumn/winter period during this experiment mean maximum and minimum temperatures outside were 24. C and 1.2 C respectively, compared with 29.4 C and 1.5 C inside the glasshouse. Watering of the pots was uniformly generous but not controlled. Ear emergence in the glasshouse began 2 weeks earlier in long photoperiods and a month earlier in short days compared with out-ofdoors. The type of fiower in each spikelet of the first panicle was determined in each plant and the length of all floral parts in three spikelets selected from the top, middle and bottom of the inflorescence was measured. Experiment 2 Plants of four lines of prairie grass were studied: Pergamino Martin Eierro from Argentina, La Estanzuela 157/49 from Uruguay, Nakura from Kenya, and the commercial strain used in the first experiment. The plants were grown singly in soil in 8-hour days until five to six leaves had appeared and then placed inside growth cabinets in photoperiods of either 11.5 or 16 hours, both at a temperature of 21^ C by day and 13 C by night. The light intensity was 35 ft-candles, provided by fluorescent tubes together with some incandescent light. Replicate pots were maintained at one of three levels of water holding capacity, 75, 5 or 25 %, by adding measured amounts of water daily. Atmospheric humidity was only partially controlled and for short periods fell to as low as 4 % from a set level of 7 % relative humidity. Eor each line there were four plants per treatment, but as there were no consistent strain differences, results are reported for all four combined. Measurements made were the same as in the previous experiment. Experiment 3 Plants of Cebadilla criolla, a line from Argentina, previously growing singly in soil in natural winter days, were placed in a heated glasshouse and maintained in a photoperiod of 12 hours. Half the pots were watered every 3 days only, the other received water continuously through a drip feed. Eollowing flower initiation, which occurred after 15 days in both treatments, the flowers of replicate plants were dissected weekly and the development of the lowermost floret in the top spikelet of the main stem recorded. 8i RESULTS Experiment i All plants grown in a photoperiod of 1.5 hours flowered wholly or partially chasmogamously, irrespective of temperature differences (Table i). Those maintained in 16-hour days were completely cleistogamous, with the exception of two plants growing outside
3 82 R. H. M. LANGER AND D. WILSON which had a few chasmogamous florets. Wherever both types of flower occurred in the satne spikelet, the cleistogamous were terminal and the chasmogatnous basal. Table i. Percentage chasmogamous and cleistogamous plants (n = 25); each sample size 25 Glasshouse Outside (max. temp C; (max. temp. 24. C; min. 1.5'' C) min. 1.2^ C) 1.s hours* 16 hours* 1.5 hours* 16 hours* Completely chasmogamous ("(, 8o 1 Partly chasmogamous (%) 2 8 Cleistogamous (" ) 1 92 * Photoperiod. Measurement of floral parts of either type showed little variation between replicate plants whether growing outside or in the glasshouse. Chasmogamous flowers had large anthers and filaments and swollen lodicules (Table 2). Anthers, and sometimes stigmas, were well extruded from the florets (Plate 2). Anthesis occurred in a large number of florets at the same time but not until the panicle was well exserted from the leaf sheath. By contrast, in cleistogamous flowers anthers, filaments and lodicules were small but the stigmas, although poorly developed, were not greatly different in length. These florets reached maturity earlier than their chasmogamous counterparts and autogamous pollination occurred shortly after emergence from the leaf sheath. Basal florets in each spikelet developed before terminal florets, except where both types of flower occurred in the same spikelet when the cleistogamous florets reached maturity first. Table 2. smeari length at anthesis of floral parts in cleistogamous and chasmogamous flowers (mm) Cleistogamous Chasmogamous."Anthers Filaments Stigmas Ovaries.7.7 Lodicules.5 i.o Experiment 2 \ ime to ear emergence was not affected consistently by water supply. Among the strains, those from South America tended to flower later than the local commercial mat^-ial. Despite careful maintenance of soil water levels, atmospheric humidity could not be accurately controlled and on occasions it fell to 4 % relative humidity for short periods. This may have prevented any plants from showing complete chasmogamy as in the previous experiment (Table 3). Nevertheless the results confirmed that cleistogamy is virtually the rule in long photoperiods irrespective of water regime but, in the shorter day length, only those plants which were kept constantly moist flowered chasmogamically. Measurement of floral parts yielded very similar values to those recorded in Table 2 and there was no evidence of differences due to strain or treatment within either type of flower. Experiment 3 Regular micro-dissection of apical meristems enabled the first visible signs of cleistogamy to be detected. In both soil moisture treatments flower initiation occurred 15 days after the beginning of 12-hour photoperiods. Further differentiation proceeded slightly faster under wet conditions so that floret development occurred about i week
4 THE NEW PHYTOLOGIST, 64, i PLATE 2 Spikelets with chasmogamous tlorets (left) and cleistottiimoiis fldri-ts R. H. M. LANGER AND D. WU.i^OS^PHOTOPERIOD/SM AND CLEISTOCJAMY IN BROMUS (./ H2)
5 Photoperiodism and cleistogamy in Bromus 83 earlier than in plants kept dry. However, once formed the latter matured more quickly than their counterparts growing under constantly moist conditions leading to earlier anthesis by about i week. As expected, flowers on plants kept constantly supplied with water were chasmogamous while in dry soil only cleistogamous flowers were formed. No quantitative differences between the two types of flower could be detected until the anthers had started to develop. Table 3. Percentage chasmogamous plants from four lines each loith four plants per treatment; results combined Soil moisture Photoperiod (hours) ( o water holding capacity) i o Thereafter, anthers of flowers developing on plants in dry soil increased in length relatively slowly but reached anthesis quickly (Table 4). Conversely, in wet soil anther growth was rapid but anthesis delayed. Table 4. Mean length of anthers of lowermost floret of top spikelet {mm) grown in a heated glasshouse zvith 12-hour photoperiod Soil moisture Days from flower initiation Dry Wet Anthesis Seed set 3-1.^.nthesis CV. (%) i DISCUSSION Flowering behaviour in prairie grass is clearly under environmental control. Of the factors examined by us, temperature appeared to have little effect, but both photoperiod and water supply had a strong influence on the type of flower produced. In long days plants were almost invariably cleistogamous, with the exception of a slight incidence of chasmogamy when water supply was abundant. In shorter photoperiods chasmogamous flowers were the rule, provided soil moisture was very high. Thus, in contrast to Stipa leucotricha (Brown, 1952), more than one environmental factor was found to determine the type of flower produced. These results thus conflrm and explain the seasonal variation in the frequency of cleistogamy recorded in Bromus carinatus by Harlan (1945) and in B. unioloides by Ragonese and Marco (1941). Furthermore, it now appears that the inability of the latter authors to obtain chasmogamy in the summer by reducing the natural day length may well have been due to insufficient soil moisture rather than differences in light intensity or temperature as compared with conditions in the spring. Our experiments also suggest that high atmospheric humidity plays a part, at least in so far that it appears to influence the degree of chasmogamy that is achieved. What is less certain is the time at which the type of flower is determined and the mechanism which is involved. Uphof (1938) considered that the condition of cleistogamy represents a flower bud which has been arrested in its normal chasmogamic development, while Harlan (1945) drew attention to the speeding up of maturation in cleistogamous flowers. Since the anthers, filaments and lodicules of these flowers are greatly reduced in
6 84 R. H. M. LANGER AND D. WILSON size, the supposition that cleistogamy is caused directly through a decrease in the growth rate of floral parts is simple and logical. However, so large an effect in a part of the plant which normally is highly buffered and protected from outside influence, for example in relation to mineral supply, remains surprising, particularly since size of the plant as a whole and of the fiowers is unaffected in prairie grass. It is also difficult to suggest reasons why the shorter anthers of cleistogamous flowers should reach anthesis earlier than their chasmogamous counterparts. Physiologically the type of ffower produced would appear to be a matter of delicate balance which Harlan (1945) attempted to explain by assuming that conditions would have to reach and maintain a certain threshold for open flowers to be formed, otherwise cleistogamy would result. Both types of fiower may appear on the same spikelet and, in individual fforets, the median anther may differ in length from the other two. In both cases the structures which differentiate first, the basal florets and the median anther, exhibit cleistogamous features. This suggests that type of flower is determined very early, probably at differentiation and well before the anthers grow in length, as found in our experiments. However, moisture at any rate appears to remain an important factor throughout the development of the fiower, as was shown in our second experiment in which despite abundant water supply only between 1 and 65 % of the florets per plant were chasmogamous, apparently in consequence of low atmospheric humidity at times. It was observed that anthers of young chasmogamous flowers were arrested in their development under these conditions and that the flowers did not open. Further work is thus required on the effect of photoperiod and moisture during floral differentiation and development and also on the ultimate mechanism involved. The observation by Leben and Barton (1957) that Kentucky bluegrass treated with gibberellic acid tends to contain more water and the report by James and Lund (i96) that treatment of winter barley with potassium gibberellate was attended by the development of enlarged anthers may provide useful indications in this respect. In Bromus, cleistogamy is apparently determined at an early stage of differentiation and therefore it is a more complex phenomenon than a mere retention of the inflorescence within the subtending leaf sheath, as in Bothriochloa decipiens in which the glume pit may prevent the exsertion of the anthers (Heslop Harrison, 1961). In the meantime it will still be possible by appropriate manipulation of photoperiod and water supply to produce cleistogamous or chasmogamous flowers, should this become necessary as part of a breeding programme. ACKNOWLEDGMENTS We wish to acknowledge with thanks receipt of a grant from the New Zealand University Grant Committee towards the cost of these experiments. REFERENCES BROWN, W. V. (19S2). The relation of soil moisture to cleistogamy in Stipa leucotricha. Bot. Gaz., 113, 438. HARLAN, J. R. (194s). Cleistogamy and chasmogamy in Bromus carinatus. Am. y. Bot., 32, 66. HESLOP H.^RRISON, J. (1961). The function of the glume pit and the control of cleistogamy in Bothriochloa decipiens (Hack.) C. E. Hubbard. Phytomorphologv, 11, 378. HITCHCOCK, A. S. (1934). New species and changes in nomenclature of grasses of the United States. Am. y. Bat., 21, 127. HUBBARD, C. E. (I9S6). Answering queries on the taxonomy and nomenclature of some grasses. Agronomia lusit., 18, 7. JAMES, N. I. & LUND, S. (i96). Meristem development of winter barley as affected by vernalization and potassium gibberellate. Agron.J., 52, so8.
7 Photoperiodism and cleistogamy in Bromus 85 LEBEN, C. & BARTON, L. V. (1957). Effects of gibberellic acid on growth of Kentucky bluegrass. Science, RAGONESE,. \. E. & MARCO, P. R. (1941). Observaciones sobre la biologia floral de la cebadilla crioua. Rev. Arg. Agron., 8, 196. RAGONESE, A. E. & MARCO, P. R. (1943). Influencia del potoperioda sobre la fornnacion de flores cleistogamas y chasmogamas en cebadilla crioua. Rev. Arg. Agron., 1, 178. RwEN, P. H. (i96). The correct name for rescue grass. Brittonia, 12, 219. UPHOF, J. C. Th. (1938). Cleistogamic flowers. Bot. Rev., 4,21.
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