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Nezv Phytol- (1994), 128, 347-362

Control of flowering and reproduction in


temperate grasses

BY O. M. H E I D E

Department of Biology and Nature Conservation, Agricultural University of Norway,


P.O. Box 5014, N-1432 As, Norway
{Received 3 June 1994)

CONTENTS
Summary 347 III. Itiflorescenee de^'eIopment 356
I. Introduction 348 IV. Inflorescence proliferation 357
II. Induction 348 V. The role of gibberellin 358
1. Terminology 348 VI. Synchronization with seasonal climatic
2. Juvenility and the flower-inducible stage 349 changes 359
3. Induction types and classification 350 References 360
{«) Species with single L D induction 350
[b] Species with dual induction
requirements 350

SUMMARY
Temperate grasses of the subfamily Festucioideae can be grouped into two main categories according to their
environmental control of flowering, species with a regular long day (LD) induction, and those with dual induction
requirements. The former group includes the temperate annual grasses and a few perennial species such as Phleum
pratense and Poa nemoralis. These species have no winter requirement and require only L D to flower.
Most temperature perennial grasses have a dual induction requirement for flowering, a primary induction which
is brought about by low temperature (vernalization) and/or short days (SD), and a secondary induction which
requires a transition to long days and is enhanced by moderately high temperatures. In most dual induction species
SD and low temperature are interchangeable and independently able to fulBl the primar\' induction requirement.
Yet, they are highly interactive in this process. Commonly the plants become day neutral at low temperature
(0-6 "C) and primary induction takes place in both SD and LD. Primary induction is then identical with the
cotnmon \ ernalization response. At higher temperatures induction becomes increasingly dependent on SD, until
a critical temperature is reached, usually c. 1218 °C, at which primary induction cannot take place regardless of
the photoperiod. In a few species, e.g. Bromus inermis, Phalaris arundinacea and to some extent Dactylis glomerata.
the SD response predominates while low temperature induction is weak or absent.
Critical temperatures and photoperiods for primary induction vary greatJy among species and, wirhiii the
species, among ecotypes of different geographical origin. Critical exposure time may vary from 3 ^ wk in arctic-
alpine Poa species to 20 wk in some Festttca species. Generally, ecotypes from high latitudes and especially arctic-
alpine ones, have wider temperature and daylength limits and require fewer inductive cycles for primary induction
than their iow-!atitude counterparts. In some grasses, especially arctic-alpine species, initiation of inflorescence
primordia takes place during SD primary induction, in others it requires a transition to LD. In the former group,
primordia are initiated in the autumn, an important adaptation to arctic-alpine conditions.
Critical photoperiods for secondary induction vary from '•J-IO h in Mediterranean ecotypes to more than 16 h,
and the critical number of L D cycles from four to eight, whereas 12-16 LD cycles are needed for the full saturated
response. Generally, high-latitude ecotypes have longer critical photoperiods and require more LD cycles for
secondary induction than do those from lower latitudes. Culm elongation, heading and inflorescence development
are all promoted by LD. The more inducti\'e cycles given and the more favourable their daylength, the greater
is the response.
Grasses also have efficient vegetative means of reproduction which are also environmentally controlled.
Vegetative proliferation of inflorescences or ' vivipary' is readily induced in habitually seminiferous grasses of both
LD and dual induction types, by marginal L D induction of flowering. On the other hand, a high proportion of
normal flowering can be obtained in habitually viviparous species and ecotypes by optimal primary and secondary
floral induction. Thus, sexuality is by no means entireK suppressed in viviparous species but is under
environmental control.
348 O. M. Heide

In the high-latitude environment the primary induction requiren:ients are met by the decreasing daylength and
temperature of autumn and winter, while the increasing daylength and temperature of spring and early summer
fulfil the secondary induction requirements. Thus, the dual floral induction control system of the temperate
perennial grasses provides an efficient and important mechanism for fitting their life cycles to the dramatic seasonal
changes of the high-latitude environment in which they hve.

Key words; Dual floral induction, flowering control, inflorescence proliferation, photoperiod, reproduction,
temperate grasses, temperature, vivipary.

and how they may modify the process into a


I. I N T R O D I." C T I O N
vegetati\'e reproduction system in some grasses.
Control of flowering time is important for the success A comprehensive re\-iew of reproduction in grasses
ofa plant in a gi\'en en\'ironment. Clinriatic factors- by Evans (1964) covers both temperate and tropical
especially daylength and temperature - are import- grasses and cereals. Readers are referred to that
ant controlling factors in this respect. The ability of review for much of tbe older literature in the field.
a plant to respond to such seasonal en\'ironmental The present review will confine itself to the herbage
signals represents an effective mechanism for fitting grasses of the Festucoideae subfamily - cultivated
the plant's life cycle to seasonal changes. and wildgrowing - of the higb-latitude and tem-
The seasonal change in daylength - identical from perate regions, emphasizing more recent work.
one year to the next - is ideally suited for this
regulatory purpose. Although its physiological im-
II. INDUCTION
portance for controlling plant development has been
1. Terminology
widely documented since the pioneering work of
Tournois (1914) and Garner & Allard (1920), its In most temperate perennial grasses the control of
ecological significance for adaptation of plants to flowering is complex, often stepwise (dual) and with
their environment is still not fully recognized. The interchangeable effects of temperature and day-
obvious reason for this is that this effect of daylength length. Induction in general can be referred to as the
is not evident until plants are transferred to another perception, transduction and transmittance of en-
latitude. Plants must be well adapted to the annual \'ironmental signals resulting in a change in plant
daylength cycle at the latitudes where they exist. developmental patterns from vegetative to repro-
otherwise they would not be able to survive, flower ductive. The inductive signal must be perceived by
and reproduce there. and is mediated in the plant by a variety of poorly
As explained below, temperature also plays an understood physiological and biocbemical processes,
important role in the control of flowering time, the nature of which is generally beyond the scope of
interacting with daylength and often determining this review. Nevertheless, we must clarify some of
the daylength response. The interaction may control their components and tetminology.
both the initial steps ofthe flowering process, leading In photoperiodic control of fiowering tbe following
to inflorescence initiation, and the speed and di- steps or component processes can be distinguished:
rection of the inflorescence's further development. (i) Photoperiodic induction - the perception of the
The highly successful grasses are no exception in pbotoperiodic signal in the leaf (Knott, 1934) ^•ia the
this regard. Their success is due to a variety of morphogenetic pigment phytochrome (Sage, 1992),
morphological and physiological characters, among and the synthesis and transport of (a) florigenic
which are the close control of flowering time and the signal(s) to tbe shoot apices (meristems). (ii) £^'0-
effective morphological protection of vegetative as cation - the processes occurring at the apex (Evans,
well as reproductive shoot apices. Thus, the 19696) after arrival of the fiorigenic principle,
developing inflorescence is enclosed by the leaf leading to (iii) Initiation of floral primordia - the
sheaths until fully differentiated and during much of morphological changes of tbe apex by whicb tbe
the culm elongation period. After heading has various parts of the inflorescence and flower pri-
occurred, each individual floret is in turn protected mordia are laid down, (iv) Inflorescence and flower
by the lemma and palea, except for the brief period dez^elopment. In grasses and rosette dicots this is
when they are forced apart by the swelling lodicules associated witb rapid stem elongation (heading or
to allow- pollen dispersal and exposure of the stigmas bolting), and (v) Anthesis.
to cross pollination, fiighly effective vegetative Often, induction takes place witbout any im-
means of reproduction of many grasses add to their mediately visible effects, and only becomes evident
success even in adverse environments. in subsequent development. Indeed, it has been
The aim of this review is to provide an overview of common to refer to induction only in this sense, as
how daylength and temperature control the various opposed to direct effects, especially of temperature
steps in the flowering process in temperate grasses, (e.g. Chouard, 1960; Lang, 1965). However, present
Flowering and reproduction in temperate grasses 349
knowledge provides little basis for such a distinction. The length of this maturation or juvenile phase
Here the term induction refers in a broad sense to all varies considerably in grasses and may even be
the effects exerted by external factors in specifically absent in some which respond to low temperature
changing the direction and/or speed of plant de- (vernalization) as germinating seeds (Cooper, I960;
velopment, whether directly or as an aftereffect. Roller & Highkin, 1960; Bommer, 1961). Vernal-
As already mentioned, flowering in many per- ization of imbibed car>'opses at 2 °C in darkness was
ennial grasses has a two step (dual) induction highly effective in primary induction of Lolium
requirement. This has further confused the ter- perenne, a minimum of 63 d being required, wbile
minology. Commonly, such plants must undergo a treatment for up to 116 d was without effect in other
winter influence before they will respond to tbe perennial grasses such as Dactylis glomerata, Festuca
correct daylength and flower. Vernalization, tbe pratensis, F. ruhra and Poa pratensis (Bommer, 1961).
effect of low temperature, was early identified with Six w-eeks of similar treatment was effective in
this response (for references see Cbouard. 1960; Hordeum bulbomm (Koller & Highkin, 1960), and
Lang, 1965). However, in a number of temperate outdoor overwintering of caryopses in 'snow-boxes'
perennial grasses SD can fully substitute for low resulted in hea\-y first-year flowering in Agropyrum
temperature in this response (see below). The term intermedium, but was witbout effect in Phalaris
"short day vernalization' has been used to refer to tuberosa (Frischknecbt, 1959). In winter rye, even
this effect (e.g. Evans, 1964). Since the term developing caryopses can be vernalized on tbe
^•ernalization is used specifically to refer to low mother plant by low autumn temperature (Gregory
temperature effects on flowering (see Chouard, & Purvis, 1938). Vernalized seeds may be dried and
1960), such confusions should be avoided. Also, sown in the field without loss of effect.
because of the dual induction requirement for Ahhough seed vernalization is possible in some
flowering in so many temperate grasses, the terms grasses like L. perenne, the rate of vernalization is
'induction' and 'induced' have been used to refer to greater in seedlings (Evans, ]960a), and many
different processes and conditions. Whereas E^-ans grasses can only he primar}" induced after some
(1964) used induction to refer to the photoperiodic growth has occurred. The length of the unresponsive
response of plants that have previously been exposed juvenile phase may vary from 2 wk in Poa pratensis
to vernalization and/or short days, Cooper (1960) (Meijer, 1984), to 4 wk in Phalaris arunditiacea
and coworkers (e.g. Cooper & Calder, 1964), re- (Heichel, Hovin & Henjum, 1980) and 5 wk in
stricted the same term to the primary effect which Dactylis glomerata (Calder, 1963; Heide, 1987) and
renders the plant able to respond to the appropriate Festuca rubra (Meijer, 1984). In Phalaris tuberosa (P.
daylength and flower. aquatica) cold treatment is effective only after several
In bis work w-itb Dactylis glomerata, which has a leaves have been formed (Ketellapper, 1960).
typical dual induction requirement, Blondon (1972) The physiological basis for the competence to
introduced the terms primary and secondary in- respond to inductive stimuli is poorly understood. In
duction oi flowering, relating to these processes. seed vernalization carbohydrate supply is essential
This terminology, clearly expressing the dual nature and excised embryos are only able to respond to cold
of floral induction in such plants, has many advan- if cultured in the presence of sugars (Gregory &
tages and has therefore been adopted by the present Purvis, 1938). This agrees with the finding that seed
author (Heide, 1980) and is summarized in Figure 1. vernalization has been successful only in grasses with
relatively large caryopses sucb as Lolium species
(Bommer, 1961), Hordeum bulbosum (Koller &
2. Juvenility and the flower-inducihle stage
Highkin, 1960) and the winter cereals (e.g. Gregory
Many plants, including many grasses, are unable to & Purvis, 1938). The size of tbe endosperm carbo-
respond to inductive conditions and to flower before hydrate poo! may thus be a limiting factor. Since
they have reached a certain age or size, tbe so-called juvenility in seedlings can be related to leaf area
'ripeness to flower' or adult stage (e.g. Lang, 1965). (Calder, 1963; Heide, 1987), accumulation of photo-
syntbates may also be essential for the competence of
SD seedlings to respond. The important role of SD for
Vegetative Primary Secondary primary induction in grasses, and its perception by
plant induced induced
tbe leaves, suggest tbat tbe photoperiodic sensitivity
Low temperature of the leaves is important. Indeed, reciprocal grafting
(LD)
experiments indicated that the inability of juvenile
plants of the dicotyledon species Bryophyllum and
Flowering
(Anthesis) Perilla to respond to photoperiod resided in the
inability of juvenile (lower) leaves to undergo
Figure 1, Illustration of the dual Horat induction pathways
common in Temperate perenniaJ grasses; alternative pri- pbotoperiodic induction and not in limitations of
mary induction by short day or low temperature (vernal- evocation at the apex (Zeevaart, 1958, 1962, 1985).
ization), follow-ed by secondary induction hy long day. Similarly, it was demonstrated in the LD grass
350 O. M. Heide

Lolium temulentum that a given area of an upper leaf by temperatures across the range 9-21 °C (Heide,
is far more effective in induction than the same area 1986a, 1992).
of lower older leaves (Evans, 1960rf). However, in After exposure to a minimum number of LD
the latter species it was also demonstrated that cycles flowering can occur in SD conditions in such
excised apices from plants of greater age had greater LD species, although at reduced rate. In Phleum
sensitivity in vitro to both a single LD given before pratertse and Poa nemoralis a minimum of two LD
excision and to gibberellins in the medium (King, cycles of 24 h is required for 50-60"o flowering,
Blundell & Evans, 1993). while four LD cycles are needed for initiation in all
plants in a sample (Ryle & Langer, 1963; Heide,
1986a). More inductive cycles are needed when the
3. Induction types and classification
photoperiod is reduced in length (Fig. 2). In Poa
(a) Species with single LD induction. Only a few nemoralis more LD cycles are needed to bring about
temperate perennial grasses have been found to flowering in subsequent 8-h tban in 12-h photoperiod
flower in response to LD alone. A prominent (Heide, 1986a), demonstrating the well-known in-
example is the obligatory LDP Phleum pratense hibitory effect of SD on flower development in LDP
(timothy) which, because of its economic import- (e.g. Evans & King, 1985). In Phippsia, a single LD
ance, has been extensively studied and documented cycle of 24 h is enough to trigger inflorescence
(Evans & Allard, 1934; Allard & Evans. 1941; development and anthesis in plants which have
Langer, 1955; Cooper, 1958; Ryle & Langer, 1963; formed fully differentiated primordia in SD, while
Heide, 1982; Junttila, 1985). Other examples are five cycles are needed for the full (saturated) response
Poa nemoralis (Cooper & Calder, 1964; Heide, (Heide, 1992).
1986 a), also an obligatory LDP, and Phippsia algida The LD response is typical also for annual grasses
which initiates inflorescence primordia in both SD of higher-latitude origin (Cooper & Calder, 1964;
and LD, but has an obligatory requirement for Evans, 1964). The 'Ceres' strain of the annual
LD for heading and flower development (Heide. Lolium temulentum of Canadian origin flowers in
1992). response to a single LD cycle of more than 18 h
These grasses have no winter requirement for length (Evans, 1 958). This plant has been thoroughly
flowering and first-year seedlings readily flower in studied (Evans, 1969a; Evans & King, 1985) and
LD without any previous exposure to low tem- because of its sensitivity and strict photoperiodic
perature or SD. \n Phleum pratense, however, Langer response it has become one of the classical model
(1956) found that tillers produced after the middle of plants for flowering studies.
April in Britain rarely produced inflorescences, and All lines of L. temulentum that have been examined
Cocks (1958) showed that cultivars differed in their are LDP. but there is variation between them both
ability to head after summer sowing due to in number of LD cycles required and in the strict-
interaction with temperature, high temperatures ness of the LD requirement. Most lines require
having an inhibitory effect on floral initiation even if more than one LD cycle (Evans & King, 1985), and
the photoperiod is adequate (Cooper, 1958; Ryle & some are even winter annuals in which flowering
Langer, 1963; Heide, 1982). This effect is strongly is accelerated by vernalization (Cooper, 1960;
augmented by even modest reductions in irradiance Peterson, Cooper & Bendixen, 1961). In the 'Ceres'
(Heide, 1982). The inhibitory effect of high tem- line the responsiveness to LD increases witb plant
perature \'aries among ecotypes and appeared to be age; whereas 12-d-oid plants required six LD
related to the May temperature of the region of cycles for floral initiation, plants aged 17, 27 and
origin (Cooper, 1958). Those adapted to northern 33 d required only four, two and one LD, re-
Scandinavian conditions were especially sensitive to spectively (Evans, 1960 c). Other annual Lolium
this high temperature/low irradiance inhibition species, as well as those of other genera of the
(Cooper, 1958; Heide, 1982). Apparently, normal subfamily Festucoideae which ba\-e been studied,
summer temperatures in Britain can be inhibitory to have also proved to be LDP (Cooper & Calder, 1964;
flowering in the fleld (Langer, 1956; Cocks, 1958; Evans, 1964).
Cooper, 1958), and the effect is enhanced by reduced
ligbt flux in late summer (Heide, 1982). Thus, (b) Species with dual induction requirements. As
shading in the field reduced flowering in timothy indicated above, most temperate, perennial grasses
significantly (Ryle, 1961). High temperature also have a dual induction requirement for flowering; a
lengthens the critical photoperiod for flowering, primary induction requirement for low temperature
while diurnal temperature fluctuations markedly (vernalization) and/or SD which enables the plant to
enhanced flowering compared with corresponding initiate inflorescence primordia, either directly in
constant temperatures (Junttila, 1985). SD or after transition to LD, and a secondary
In Poa nemoralis and Phippsia algida no inhibitory induction requirement for LD allowing for culm
effect of high temperature was observed on LD elongation, inflorescence development and anthesis.
induction of flowering which was almost unaffected Such plants may correctly be referred to both as
Flowering and reproduction in temperate grasses 351

10 H

5 -

Number of cycles
Figure 2. Effects of photoperiod length and number of inducti\ e cycles in the long da>' plant, Pua nemoralts.
Number of heading plants out of 10 in each treatment (Heide, l9Hba).

short-long-day plants and long day plants with a 1), and may also vary much among ecotypes of
vernalization requirement (cf. Fig. 1). different geographic origin within the same species
Basic to the understanding of flowering control in (e.g. Habjorg, 1978; Heide, 1980, 1988 a). Generally,
the dual induction grasses, is tbe fact that the ecotypes from high latitudes and especially arctic-
primary induction effect is local, i.e. induced tillers alpine ones, have wider temperature and daylengtb
cannot induce later-formed adjacent tillers. In other limits and require fewer inductive cycles for primary
words, the stimulus or whatever change produced m induction than their low-latitude and maritime
primary induced tillers is not transmissible to other counterparts.
apices. In perennial grasses tberefore the primary Among the species with the least requirements for
induction needs to be repeated every year, each primary induction are arctic-alpine Poa species and
individual tiller having a biennial and monocarpic ecotypes (Heide, 1980, 1989a, 6) and Alopecurus
life cycle. pratensis (Heide, 19866). In high-arctic ecotypes of
Temperature and daylength are highly interacti\ e Poa alpina and P. alpigena from S\ albard, 3-4 wk
in the primary induction process. In most species the exposure to 3-6 °C in 8 b photoperiods was sufficient
general pattern is that tbe plants become day neutral for primary induction (Heide, 1989«), while in high-
at low temperatures (0-6 °C), and under these latitude ecotypes of Poa pratensis and Alopecurus
conditions primary induction is identical with the pratensis, 6 wk at the same conditions were required
common vernalization response (e.g. Chouard, 1 960; (Heide, 1980. 1986^). With extended exposure time,
Lang, 1965). However, as temperature rises, primary induction was obtained in tbese species at tempera-
induction will occur in SD only, until a certain tures up to 12 °C in 24-h photoperiod and up to
threshold temperature level is reached, above which 18 °C in short days of less than 12 h duration (Heide,
primary induction cannot take place regardless of the 19866, 1989a).
pbotoperiod and duration of treatment. This dy- An interesting point is, however, that the higb-
namic interaction of temperature, photoperiod and arctic Poa species from Svalbard which hardly ever
exposure time is well demonstrated on Poa pratensis experience short days in a non-frozen condition,
(see Fig. 3; Lindsley & Peterson, 1964; Heide, have retained such a strong SD response. This was
1980). Although SD and low temperature are found also in Cerastium regelii, a high-arctic dicot
independently able to bring about the primary species from Svalbard (Heide, Pedersen & Dabl,
induction response, their effects are additive when 1990). Such a SD response is apparently of little
applied sequentially, especially if the SD treatment adaptive value in the high-arctic environment and is
is applied first (Heide, 1980, 1988o). probably a relict character (with no negati\'e fitness
Critical temperatures and daylengtbs, as well as effect) inherited from ancestors at lower latitudes.
the critical duration of exposure for primary in- Another species in this group is Bromtis inermis in
duction vary greatly among the grass species (Table which primary induction takes place in SD at
352 O. M. Heide

- 5

12

Figure 3. Interaction of temperature, photoperiod and exposure time in primary induction of Poa pratensis cv.
Holt. Five-wk-old seedlmga were exposed to photoperiods of 10 {%), 16 (O) and 24 (D) h at temperatures
ranging from 3 to 12 °C for 6, 8 or 10 wk. Ordinates indicate number of flowering plants out of 10 and mean
number of panicles in each treatment in subsequent 24-h photoperiod at 21 "C (Heide, 1980, with
permission).

temperatures ranging from 6 to 24 °C with an Lofar. The latter also had somewhat lower tem-
optimum response at 15-21 °C (Heide, 1984). At perature optima (Heide, 1984, cf. Fig. 4).
such optimal temperatures 4—6 wk of SD treatment An intermediate primary induction requirement is
are optimal for primary induction, whereas no found in Dactylis glomerata (Heide, 1987), Festuca
induction takes place in 24-h LD at 3 °C even with vivipara and F. ovina (Heide, 1988a), and Phleum
16 wk of treatment. This species, unlike most other alpinum. (Heide, 1990fl). These species require
perennial temperate grasses, appears to have a 8-12 wk of exposure to optimal conditions for
specific SD requirement for primary induction primary induction, but they vary considerably with
which cannot be replaced by low temperature respect to the range of inductive conditions. In three
vernalization in LD (cf. Fig. 1). Critical photoperiods Scandinavian cultivars of D. glomerata full induction
for primary induction at 15 and 24 °C, respectively, was obtained at temperatures of up to 18 °C in 8-h
were 13-5 and 12 h in the North-American cv. SD (10 wk exposure) and 50% flowering even at
Manchar, and 14-5 and 13 h in the Norwegian cv. 21 °C In 24-h LD, however, induction was re-
Flowering and reproduction in temperate grasses 353

Table 1. Primary induction requirements for fiowering in some temperate


perennial grasses

In short days (< 12h) In long days (> 16 h)

Temperature Exposure Temperature Exposure


Species (°C) (wk) CO (wk)
Poa alpina 3-18 4-10 3-15 6-10
Poa alpigena 3-18 4-8 3-12 6-10
Poa pratensis 3-18 6-10 3-12 8-12
Alopecurus pratensis 6-18 6 6-15 6-8
Bromus inermis 6-24 4-6 n.i. n.i.
Dactylis glomerata 9-21 8-10 0-3 >20
Phleum alpinum 3-15 9-12 3-12 12-14
Festuca vivipara 3-15 10-18 3-6 10-18
Agrostis capillaris 3-12 15 3-6 15
Phalaris arundinacea 3-15 12-18 n.i. n.i.
Lolium perenne 3-? 12-16 3-? 12 16
Festuca pratensis 3-15 16-20 3-12 18-20
Festuca rubra 6-15 12-20 3-12 20

Ranges of exposure time requirements indicate variation with temperature


and geographic origin of ecotype/cultivar.
n.i., no induction.

100

Primary

50

'Manchar'

1 9-^f

24 8
Photoperiod (h)
Figure 4. Photoperiodic requirements for primary and secondary induction offioweringat 1 5 and 24 °C in two
cultivars of Bromus inermis (Heide, 1984, with permission).

stricted to 3 °C and required more than 20 wk of pratense subsp. bertelonii (syn. P. nodosum) resembles
exposure. These results confirm the conclusions of P. alpinum in this respect. Thus, even taxonomically
Calder (1963, 1964) and Hroue & Nicholls (1973) closely related grasses may differ much in their fioral
that SD alone is sufficient for primary induction in induction requirements.
D. glomerata, and that at no stage of development is The most extreme primary induction require-
any cold needed for fiowering in tbis species as has ments are found in the genus Festuca (Bean, 1970).
been claimed in several reports (for references see In three Scandinavian cultivars of F. pratense
Heide, 1987). Blondon (1972) found that even high 16-20 w^k at 6 °C in 10 h photoperiods were needed
temperature (27 °C) at bigh light intensities could for 'saturation' of primary induction (Heide, 19886).
bring about primary induction in a clone used by Whereas 9 °C was optimal (and 12 °C effective), for
him. A point of interest is that the alpine timothy induction in 8-b SD, temperatures of 3-6 °C were
(Phleum alpinum) has a dual induction requirement, required for induction in continuous light. Similar
wbile tbe cultivated bexaploid timothy requires LD results were obtained in Norwegian F. rubra eco-
only for flowering. The results by Cooper & Calder types, although w ith a larger variation among ecotypes
(1964) indicate tbat the closely related diploid P. (Heide, 19906). Thus, while an ecotype from North
354 O. M. Heide

Norway reached full induction within 15 wk of induction response, but only temperatures of 12 °C
exposure to 6 °C/SD and with 21 wk at 6 X / L D or below and daylengths of 8 or 16 h were highly
(24 h). an ecotype from South Norway needed 21 wk effective. At 3 and 6 °C induction took place even in
for the same response at 6 °C/SD and had only 24-h photoperiod, Again, 9 °C was the most effective
marginal induction with 21 wk at 6 °C/LD. The temperature in SD; this seems to be the case for a
variable response may at least in part be due to the number of temperate grasses (Heide, 19906). Pre-
taxonomic complexity of this tax on. As witb 7^. liminary experiments with Deschampsia species [D.
pratense, 9 °C was the optimal temperature tor SD caespitosa, D. alpina, D. f}.exuosa) indicate that tbey
Induction in ail F. rubra ecotypes (Heide, 1990^). all fall into this category with an extreme primary
Similar extreme primary induction requirements induction requirement (Heide, unpublished results).
were demonstrated in F. arundinacea (Bean, 1970). The extent of the primary induction requirement
To this group belongs also the late-flowering is also reflected in the time and progress of floral
(higher-latitude) types of Lolium perenne. Tbe pri- initiation of the grasses in the field. In an extensive
mary induction requirements vary greatly withm the study conducted hy Bommer (1959) in Germany,
species, and plants of Mediterranean origin may Alopecuruspratensis was the earliest species to initiate
even have none (Cooper, 1960). In the late-flowering floral primordia in the autumn followed by Antho-
British strain S.23 E\-ans (1960fl, h) found that about xanthum odoratum whereas Phalaris arundinacea,
12 wk of SD treatment at 4 °C were required for full Agrostis alba, Lolium perenne and the Festuca species
response, using 16 wk as a standard 'vernalization' were among the latest, with initiation in tbe spring.
treatment. The rate of primary induction increased However, in many dual induction grasses no
with increase in temperature from 4 to 10 °C (Evans, morphological changes take place at the apex during
1960o). Details on temperature ranges for induction SD primary induction. In otber words, primary
in SD and LD are, however, missing for this induction alone does not trigger floral initiation,
economically very important species. which only takes place after a shift from short to long
The linkage between primary induction require- days. This has been demonstrated in one group of
ments and perenniality has been beautifully demon- grasses including Lolium perenne (Evans, 1960a),
strated in the genus Lolium (Cooper, 1960; E\'ans, Brrjmus inerniis, Dactylis glomerata, Festuca prat en sis
1960a). Thus, tbe induction requirement varies and F. rubra., Phleum alpinum (Heide, 1984, 1987,
from obligatory and large in L. perenne through 19886, 1990a, 6) and Phalaris arundinacea (Heide,
facultative and intermediate in hybrids of L. unpublished). Cultivars within a species may, how-
perenne x L. multiflorum and in biennial types of L. ever, differ in this respect as Niemelainen (1990),
multiflonim (Italian ryegrass), slight in winter annual found that in Dactylis glomerata the Finnish cv.
types of L. multiflorum and L. rigidum (Wimmera Haka initiated inflorescence primordia in both
ryegrass), to none in the typical summer annual natural and artificial SD. On the other hand,
strains of L. multiflorum (Westerwalds ryegrass) and cultivars of F. pratensis (Heide, 19886) and P.
L. temulentum (Cooper, 1960; Evans, 1 9 6 0 G ) . arundinacea did not initiate inflorescence primordia
Large primary induction requirements are also in SD at 6-9 °C even after 27 and 31 wk of exposure,
found in Phalaris arundinacea and Agrostis capillaris respectively, whereas initiation was immediate after
(syn. A. tenuis). In the P. arundinacea cultivars transfer to LD. With such over-induction some
'Vantage' and 'Rise' 12-15 wk at 6 °C in 8 h apices die and the number of developing inflores-
photoperiods were required for full response cences is actually reduced.
(Heichel et al., 1980). Photoperiods of 16 b at the In contrast to this is the completion of inflorescence
same temperature were less effective. While the initiation and differentiation which takes place
results with 'Vantage' were confirmed, Norwegian during SD induction in another group of northern
cultivars and breeding lines of P. arundinacea grasses with a relati\-ely small primary induction
required up to 18 wk at 6-9 X 7 8 h photoperiod for requirement. This is the case with northern ecotypes
full induction (Heide, unpublished results). In SD of Poa pratensis (Habjorg, 1979; Heide, 1980) and
primary induction was effective over the 3-12 "C other arctic-alpine Poa species (Heide, 1989a), as
temperature range (somewhat less at 15 °C), with an well as Alopecuruspratensis (Heide, 19866), Hordeum
optimum at 9 °C. In 24-h phutoperiods induction bulbosum (Roller & Higbkin, 1960) and certain
was virtually absent at these temperatures. These cultivars of winter wbeat (Evans, 1 987). In all these
responses are in contrast to those of Phalaris aquatiea species tbe complete inflorescence primordia, up to
(syn. P. tuberosa) which is equally well vernalized in the terminal spikelet, are formed while the plants are
short and long days (Cooper & McWiUiam, 1966; still in SD (stages 5-6, Jeater, 1956). Thus, although
McWilliam. 1968) and has a much shorter exposure the environmental requirements for flowering are
requirement (Ketellapper, I960). similar, the actual control point in tbe differentiation
In experiments with Norwegian ecotypes of cycle is different in those two groups of grasses.
Agrostis capillaris Karlsen (1988) found that at least In their bigh-latitude environment the latter group
15 wk of exposure were required for full primary of grasses initiate floral primordia in the autumn, a
Elowering and reproduction in temperate grasses 355

feature which has also been demonstrated in Alaskan intermediate temperatures in LD as in some of the
grasses (Hodgson, 1966). This seems to be an above examples (cf. Eig. 1), there is in fact no dual
important adaptive strategy to a short and cool induction. In LD at such temperatures induction,
growing season (Heide, 1985). ln Poa pratensis a initiation, heading and anthesis proceed uninter-
marked latitudinally determined ecotypic differen- ruptedly in one continuous sequence. Induction may
tiation is found in this character {Habjorg, 1979; then be considered a normal LD response similar to
Heide, 1980). Similar differences are found among that of Fhleum pratense. Such diverse responses
Festuca vivipara ecotypes (Heide, 1988«). Although make response-type classification according to class-
autumn initiation clearly is associated with a small ical terminology rather complicated and suggests
induction requirement (Bommer, 1959; Heide, 1980, that the various responses have much in common
1989(7), it is not a direct result of it since a transition and simply represent modifications of the same
from SD to LD is clearly required for fioral initiation o\erall multiple flowering control mechanism (cf.
in many species and ecotypes. Evans, 1969; Bernier, 1988).
In nearly all grasses with dual induction require- After the primary induction requirements have
ments, with the exception of Bromus inermis (Heide, been met, whether by short days or low temperature
1984) and possibly Phalaris arundinacea (see above), (vernalization), secondary induction by long days is
SD and low temperature (vernalization) are inter- necessary for normal flowering in the dual induction
changeable in their effects and will independently grasses. The response ai Bromus inermis presented in
of each other bring about the primary induction Figure 4 is a typical example. With some notable
response (cf. Fig. 1). This has also been demonstrated exceptions discussed above, fioral initiation is trig-
in winter annuals hke winter rye (Purvis & Gregory, gered by the transition from short to long days, ln
1937) and certain cultivars of winter wheat (Evans, most species this LD requirement is obligatory for
1987), as well as in the biennial and perennial dicots inflorescence development, but in some arctic-alpine
Campanula medium (Wellensiek, 1985), Scabiosa species and ecotypes heading and anthesis may take
succisa (Chouard, 1960) and Cerastiutn regelii (Heide place slowly, also in SD, especially at higher
et al, 1990). temperatures. Examples are northern ecotypes of
This raises the question of the specificity of the Foa pratensis and other northern Poa species,
vernalization and photoperiodic responses (Heide, Alopecurus pratensis, Eestuca ovina and Fhteum
1986/j, 1987, 19886; Evans, 1987). Since the photo- alpinum {Heide, 1980, 1989«, 19866, 1988a, 1990fl).
periodic signals are perceived by the leaves (Knott, With the exception of Phleum alpinum these are the
1934; Lang, 1965) while vernalizing temperatures same grasses which initiate floral primordia while
act directly on the shoot apex (Purvis, 1940; Lang, still in SD (see abo\-e).
1965), it has been assumed that photoperiodism and Critical photoperiods for secondary induction
\'ernalization are basically different phenomena. Yet, range from 9-10 h in Mediterranean ecotypes, to
their effect in primary induction is the same; both more than 16 h. Usually, ecotypes of high latitude
enabling the plants to respond to and flower in origin have the longest critical and optimal photo-
subsequent LD, suggesting that at least their end periods (Cooper, 1960; Pringle, Elhot & Degenhardt,
products are similar or even identical. However, as 1975; Habjorg, 1978; Heide, 1984, 1987, 19886;
discussed by Evans (1987), several lines of evidence Karlsen, 1988), and require the highest number of
indicate the utilization of different pathways by the l^D cycles for secondary induction (Heide, 1984,
two induction processes. 1987, 19886).
It may be argued that these examples are only The temperature effect on secondary induction
special cases of the well-known interaction ot differs between species. In those species forming
photoperiod and temperature in the induction of inflorescence primordia during SD primary induc-
flowering, whereby a number of SDP become day tion high temperature (21-24 °C) can to some extent
neutral at lower temperatures (see e.g. Lang, 1965; substitute for the LD requirement of secondary
Bernier, Kinet & Sachs, 1981). ln particular, when induction (Heide, 1980, 19866, 1988«, 1989a),
the temperature range for primary induction in LD whereas the species in which initiation requires a
is as wide as in Alopecurus pratensis and some Foa transition from SD to LD show the opposite
species (Heide, 19866, 1989a), it is difficult to argue response, the critical photoperiod will increase with
for two entirely different processes in LD and SD. Is the temperature (Evans, 1964; Heide, 1984, Fig. 4).
this effect of low temperature merely to render the Devernalization by high temperature will occur in
plants insensitive to photoperiod in the primary these species if primary induction is marginal or
induction process? The fact that the SD response incomplete (Evans, 1964; Heide, 19886).
always is reduced in effectiveness at the lower The degree of primary induction is also of great
temperatures which are optimal for vernalization importance for the secondary- induction requirement.
response (0-6 °C) lends support to this possibility The more complete the primary induction, the less is
(cf. Cooper, 1960). Furthermore, it should be the critical secondary induction requirement, i.e.
observed that when primary induction takes place at fewer LD cycles or shorter photoperiods can trigger
356 O. M. Heide

secondary induction (Evans, 1960a; Peterson el a}., reduced flowering in the single-induction L D P
1961). This suggests that primary induction in some Phleum pratense (Ryle, 1961).
way increases the responsiveness of the shoot apex to The role of sugars in floral induction has been a
substances translocated from the leaves in LD matter of contention (e.g. Bernier, 1988). However,
conditions (Evans, 1964). It is also in agreement with a careful recent study of photoperiodic and photo-
tbe classical vernalization concept that the role of synthetic effects on apical sugar content in Lolium
vernalization is to render the plants responsive to temulentum (King & Evans, 1991), revealed tbat
subsequent photoperiodic induction (e.g. Lang, photoperiodic time measurement and induction in
1965). the leaves as well as evocation at the apex were
The critical number of 24-h L D cycles re- independent of and unaffected by pfd and sucrose
quired for secondary induction in fully primary- availability at tbe apex. On the other band, inflores-
induced plants of many grasses ranges from about cence development was highly responsive to bigh
four to eight cycles, whereas 12-16 LD cycles are sugar availability (King & Evans. 1991). Therefore,
required for the full response (Evans, 19606; Heide, the effects of defoliation and low pfd on floral
1984, 1987, 1989fl. 6. 19906). Even in those arctic- induction and evocation in grasses seem to be non-
alpine species in whieh flower development may specific, a favourable carbohydrate status being a
also take place in 8-h SD, there is an increasing prerequisite for normal photoperiodic and thermal
response with up to 12-16 LD cyeles (Heide, 1989fi, responses and for production of a high number of
1990fl). responsive tillers. Also the grow-th and rate of
Low light intensities are photoperiodically effec- development of induced tillers increase under high
tive and, as in other LD plants, a high proportion of pfd (King & Evans, 1991).
far-red light is optimal for day-length extension Nitrogenous fertilizers applied before the onset of
(Vince-Prue, 1975). Eor all the grasses studied by primary induction increase the number of inflores-
the present author about 2 //mo! nn"'^ s~^ (400-700 nm cences in several dual induction grasses (Evans &
range) supplied b\' incandescent lamps has been Wilsie. 1946; Sprague. 1948; Peterson & Loomis,
adequate for extension of 8-10 h of daylight or high- 1949; Newell, 1951; Calder & Cooper, 1961;
intensity fluorescent light. About 1 3//mol m"^ s"^ Aamlid, 1993). Again, the effect is mainly indirect
was sufficient for daylength extension in Phleum through an increase in the number and vigour of
pratense (Cooper, 1958). and about 3-3 /imol m"^ s"' induceable tillers in the autumn (Meijer & Vreeke.
in Dactylis glomerata and species of Lo/mm (Sprague, 1988; Aamlid, 1993).
1948; Cooper, 1956). Nij^iht interruptions near the
middle of tbe dark period have been effecti\'e in LD
111. INFLORESCENCE DEVELOPMENT
secondary induction in several dual induction grasses
(Sprague. 1948). Our experience is, how'ever, that Development of fully differentiated inflorescence
such night breaks should last tor at least 1-2 h to be primordia is essentially a growth process, and as
fully effective in the grasses (Heide, Bush & Evans, sueb, highly influenced by temperature. Time to
1985). heading decreases with increasing temperature dur-
In addition to the main control b)' photoperiod ing this stage, at least up to about 25 °C. Never-
and temperature, botb primary and secondary in- theless, culm height, panicle size and usually also
duction are modifled and may be limited by other final inflorescence number w^ill be largest at relatively
external factors. Notable in this respect is the effect low teinperatures (12-15 '^C).
of photon flux density (pf'd). Thus, primary in- In all high-latitude perennial grasses inflorescence
duction, both in the classical vernalization sense and development is also strongly stimulated by long
by SD, is highly dependent on adequate light days. Although heading may take place in 8-h SD in
conditions and a favourable carbohydrate status of some species (see above), the development is slow, a
the plants to be effective (see Lang, 1965; Bernier et high proportion of the primordia abort, and those
al., 1981). Experiments in artificial ligbt conditions developing are stunted w ith very short culms (Heide,
must take this into account. The need for a high 1980, 19866, 1988a, 1989a, 1990a). The com-
carbohydrate/energy status was clearly demon- bination of SD and cool temperatures during tbe
strated by dramatic reductions of flowering caused period following completion of primary induction is
by moderate defoliation before onset of primary strongly inhibitory to culm elongation. Eurthermore,
induction under greenhouse conditions in both Poa this inhibitory effect is irreversible and cannot be
pratensis (Peterson & Loomis. 1949) and Phalaris overcome by subsequent LD conditions (Heide,
arundinaeea (Heichel et al., 1980). Autumn mowing 1980). Thus, in Poa pratensis cv. Holt, intercalation
also reduced seed yields m first year seed production of a 6-wk SD period between primary induction for
leys of Poa pratensis, but was beneficial in older leys. 10 wk at 3 ° C / 2 4 b pbotoperiod and flower de-
probably by improving the ligbt conditions for the velopment at 21 °C/24 h reduced final culm height to
new tillers in the dense older stands (Aamlid, 1993). only 30 °o of that of plants which went directly into
Reduction of natural light conditions in the field also LD/high temperature. However, when the same
Flowering and reproduction in temperate grasses 357

treatments were given in the reverse order SD were abnormality or error of development in the habitually
highly stimulatory. Inhibition was maximal at in- non-viviparous (ephemeral) grasses is the normal
termediate temperature (12 °C) and increased sharp- situation and has become genetically assimilated in
ly at daylengths below 16 h (Heide, 1980). These viviparous species to the extent that it is referred to
effects are very pronounced also under field condi- as a form of apomixis (Stebbins, 1941).
tions when northern ecotypes of P. pratensis are It is often observed that habitually seminiferous
transferred to lower latitudes where SD conditions grasses develop viviparous mflorescences when
prevail in early spring, particularly in years with developing in late summer and autumn (for early
early snowmeh (Habjorg, 1978, 1979; Heide, 1980). references, see Evans, 1964). Numerous experimen-
This has important implications for choice of area tal studies indicate that this is due to the decreasing
for commercial grass seed production (Heide, 1980; photoperiod and temperature late in the season
AamlJd, 1993). (Wycherley, 1954; Evans. 19606; Junttila, 1985;
The intensity of secondary induction in dual Heide 1986a, 1987, 1988fl, 1989a, 19906). Such
induction grasses also has a strong effect on rate of ephemeral \'ivipary occurs in single induction L D
inflorescence development. The more inductive grasses such as Fhleum pratense (Nielsen, 194] ;
cycles given, and the more favourable their day- Langer & Ryle, 1958; Junttila, 1985) and Foa
length, the greater is the rate of subsequent inflores- nemoralis (Heide, 1989a), as well as in many dual
cence development (Evans, 19606; Heide, 1980, induction grasses (see Evans, 1964; Heide, 1989 a).
1984, 19866, 1987, 1988a, b, 1989a, 199()Q, 6, 1992). The most important environmental regulatory factor
The same applies to single induction LD grasses is dayiength. Marginal LD induction, both in the
(Evans, 1958; Heide, 1982, 1986 a) and the rate of form of marginally inductive photoperiods (Junttila,
inflorescence de\'elopment provides a sensitive index 1985; Heide, 1988a), and of a marginal number of
of the intensity of induction in both groups (Evans, fully inductive LD cycles (Wycherley, 1954; Evans,
1958, 19606). Under marginal or unfavourable 19606; junttila, 1985; Heide, 1986o, 1987, 1988a,
dayiength conditions primordia may undergo im- 1989a, 19906), commonly induces inflorescence
perfect development resulting in \'egetative pro- proliferation in habitually seminiferous temperate
liferation of the inflorescences. grasses. The effect can be modified by temperature.
Eor example in P. pratense, in which the critical
photoperiod increases with increasing temperature
IV. INFLORESCENCE PROLIFERATION (Heide, 1982; Junttila, 1985) the proportion of
Asexual reproduction is widespread and important proliferating in/iorescences increased u'hen the tem-
in many temperate and high-latitude grasses. In perature was increased under marginal photoperiodic
many arctic-alpine Poa species three different asexual conditions (Junttila, 1985). In other species in which
mechanisms are often at work within the same LD induction is most effective at high temperatures,
population, namely vegetative spread by rhizomes, low- temperatures during LD induction ha\-e the
inflorescence proliferation ('\'ivipary'), and apos- same effect (Youngner, 1960; Heide, 1988a).
pory. Combinations of these w ith the various asexual Similar 'vegetative inflorescence' phenomena are
breeding strategies result in the complex genetic known also in other plants with different environ-
structures of many grass populations. Richards mental requirements for flowering, e.g. the SD plant
(] 990) has review ed the diversity of breeding systems Kalanchoe blossfeldiana (Harder, 1953), the low
in grasses and their implications for the genetic temperature-dependent Ereesia x hybrida (Heide,
architecture of grass populations. The environmental 1965), and the long-short-da>' plant Bryophytlum
influence on and regulation of these mechanisms will daigremontiartum (Zeevaart, 1985). In all cases pro-
be highlighted here. liferation is associated with marginal floral induc-
Application of the term vivipary to proliferation of tion ; in the case of Bryophyllum proliferation was
spikelets has led to some confusion as has been produced also by marginal induction by gibberellin
thoroughly discussed by Latting (1972). In the strict in SD. It can thus be concluded that the ephemeral
sense the term is applied to mean germination of vivipary in habitually seminiferous grasses as well as
seeds while still attached to the parent plant (Arber, other forms of '\'egetative inflorescence' formation
1934; Hartman & Kester, 1975). Here it is used in are the results of marginal or incomplete floral
the sense of Latting (1972) as 'the development of induction. In extreme cases a complete reversal to
vegetative shoots among the reproductive organs'. vegetative conditions may occur, leafy shoots being
According to Latting (1972) two types of meristems formed at the top and/or nodes of the culms instead
are involved in the proliferation process, the apical of inflorescences (cf. Karlsen, 1988).
meristem ofthe spikelet and the intercalary meristem On tbe other hand, a large proportion of normal
of the lemma. These meristems are activated and flowering was obtained in habitually vi\iparous
give rise to leafy organs and plantlets, while the forms oi Eestuca vivipara, Poa alpina and F. alpigena
sexual parts usually abort. As pointed out by Arber by optimal floral induction, both primary and
(1934) and Evans (1964), what is essentially an secondary (Heide, 1988 a, 1989 a). Both dayiength
358 O. M. Heide

and temperature effects on flowering were demon- remained vegetative when rooted and grown in
strated in all species. A complete shift to normal subsequent LD (Heide, 1988 a). Apparently, such
flowering was not observed in any species, however. plantlets are in a juvenile state and only become
That sucb flowers may be reproductively functional receptive to primary induction after root formation
was suggested by positive pollen staining tests in F. and production of some growth, whereas attached
vivipara (Heide. 1988a) and Salvesen (1986) found plantlets respond to hormonal stimuli produced by
varying degrees of seed production in tetraploid the parent plant. Such observations support the
populations of this species after open pollination in hypothesis that the limitations of juvenile plants
an esperimental garden. reside mainly in their inability to produce flowering
Such findings clearly demonstrate tbat sexuality is hormone(s) and not in an ability to respond to such
by no means entirely suppressed e\-en in the stimuli (cf. Zeevaart, 1962).
'obligatory' viviparous species, but that it is under
environmental influence, as suggested by Evans
V. THE ROLE OI' GlBBEHtLElN
(1964). By these mechanisms, viviparous species can
benefit from the advantage of a highly efficient The effects of gibberellin (GA) on flowering have
vegetative reproduction method under marginal been extensively reviewed by Lang (1965). Zee\'aart
climates in arctic-alpine areas, and still retain the (1978) and Pharis & King (1985). The responses of
possibility of genetic recombination allowing for various plant groups and species are both diverse and
evolution and adaptation to a changing environment. complex, but some general features are apparent: (a)
Witb such an 'optimal versatility' it is understand- GA can substitute for LD in many herbaceous LDP
able that vivipary has been such a common and and in tbe LSDP Bryophyllum daigremontianuni
successful adaptation to arctic-alpine environments. when grown in SD (Zeevaart, 1985). (6) GA can also
Of special significance is that a condition such as SD substitute for low temperature (vernalization) m
whieh favours vivipary is also seasonally linked to a many cold-requiring plants (Lang. 1965). (c) In SDP
temperature regime that makes this form of re- GA is usually ineffective or even inhibitor^', although
production of special advantage. Long days on the there are exceptions like Chrysanthemum, Impatiens
other hand, favouring flowering, are linked to the and Pharbitis (Pharis & King, 1 985). {d) Inhibitors of
early part of the grow ing season when the potential gibbereliin biosynthesis (growth retardants) may
for completion of seed development and maturation inhibit LD induction and exogenous GA may
would be best (Heide, 1988a). overcome tbis inhibition.
The experimental results with both seminiferous In the annual LD grass Lolium temulentum
and viviparous species agree with the hypothesis of exogenous GA applied to leaves or to the apex
WVcherley (1954), that a greater amount or con- induces flowering under non-inductive SD condi-
centration of flowering hormone(s) is needed for tions (Evans, 1969fl). Furthermore, apices excised
normal flow^ering than for \iviparous proliferation. from 7-8-wk-oid plants grown at bigh irradiances in
In this connection it should be noticed tbat induction SD could undergo inflorescence differentiation in
and heading in vi\ iparous species was controlled in vitro when GA was provided in the medium (King et
the same way and had the same dual induction al. 1993). The order of effecti\'eness of gibberellins
requirements as in their normal flowering counter- w^as 2.2-dimethyl-GAj > GA^ > GA^ > GA,, tbe
parts (Heide, 1988a, 1989a). same ranking as found for intact plants (Evans et al.,
Induction of proliferation by growth substances 1990). Applications of GAy to leaves before apex
has also been demonstrated. Spraying with auxin- excision could substitute for GA in the medium, and
type herbicides induced proliferation in several apices from plants given one LD reached high floral
grasses (Jeater, 1958), and cytokinin was very scores even w'hen there w"as no GA in the medium.
effective in inducing \-ivipary in aseptically cultivated The presence of GA in the medium was not required
inflorescence primordia and inflorescences oi Phleum until 4—6 d after excision from plants given one LD,
pratense (Junttila, 1985). Tbe auxin 2,4-D, on the and appeared to be necessary for differentiation
other hand, stimulated root formation at low concen- beyond the spikeiet primordia stage (King et al.,
trations and at higher concentrations it induced 1993). On tbe basis of these results the authors
callus growth, thus preventing spikeiet development conclude tbat at present it is not possible to tell
(Junttila, 1985). whether the LD stimulus to flowering in L. temu-
It can sometimes be observed that miniature lentum actually is a GA, or whether a GA is a
viviparous plantlets of obligatory viviparous species component of the stimulus or is acting synergistically
may head and de\eiop a new generation of proli- with it (King et al., 1993).
ferated inflorescences wbile still attached to tbeir In the dual induction grasses Poa pratensis cv.
parent plants. However, such development could not Holt and Bromus inermis cv. Manchar, application of
be induced in detached viviparous plantlets of F. GA., during primary induction was strongly in-
vivipara, even by extended primary induction treat- hibitory to flowering (Heide, Bush & Evans, 1987).
ments by low temperature and SD. but plantlets In P. pratensis weekly spraying with 1 x 10"* M
Flowering and reproduction in temperate grasses 359

during SD treatment at 9 °C for 10 wk completely However, there is accumulating evidence for im-
suppressed primary induction. Lower concentrations portant roles of gibberellin in the control of flowering
down to 1 X 10"^ M also caused significant inhibition, in both LD and dual induction grasses. Unravelling
especially with shorter induction periods. In Bromus these effects is important for the understanding of
inermis the same GA;, treatments inhibited primarv- the control of flowering in general.
induction in plants exposed to SD at 18 °C for up to
6 wk (Heide et al., 1987). Similar inhibitory effects
VI. SYNCHRONIZATION WITH SEASONAL
were obtained with Arrhenatherum elatius (Bommer,
CLIMATIC CHANGES
1964). Although the concentrations applied were
high, they may not have exceeded physiological An inevitable consequence of the dual floral in-
concentrations which reach as high as 3 x 10"'' M in duction requirement of most temperate grasses and
the shoot apex of Lolium temulejituni (Pharis et al., the monocarpic nature of individual tillers is that
1987). each tiller has a biennial life cycle. Therefore, the
Since both GA and non-inductive LD conditions potential of these grasses for flowering and seed
greatly stimulate elongation in these and other production in any year is determined b}' the size of
temperate grasses (Hay & Heide, 1983 ; Heide et al., the population of receptive tillers at the time when
1985 ; Hay, 1 990), the degree of primary induction is the combination of temperature and daylength
negatively correlated with plant height (leaf sheath becomes favourable for primary induction in the
and blade length). The GA biosynthesis inhibitor autumn of the previous year. This is the physio-
CCC which effectively reduces leaf growth of these logical basis for the important and widely recognized
grasses (e.g. Heide et al., 1985) also enhances practice of renewing seed production fields by
primary induction of flowering especially under burning or mowing and application of nitrogen
marginal conditions (Buettner, Ensign & Boe, 1976; fertilizers in late summer and autumn.
Heide, unpublished results). Also, experiments in At high latitudes, where the onset of SD is late and
Norway with autumn application of CCC have given frost comes early in the autumn, tbe frost-free SD
promising seed yield results in seed production leys primary induction period will necessarily be short or
of Bromus inermis, a species which tends to get may even be absent (see Fig. 5). Under such
marginal SD primary induction in high latitude conditions the alternative LD/low temperature by-
environments (Klebesadel, 1970; Heide, 1984). pass is of particular importance for facilitation of
These results and others relating to the daylength primary induction (Fig. 1). Species and ecotypes
control of important steps in the GA intereonversion adapted to such conditions, e.g. arctic-alpine Poa
pathway (Gilmour et al. 1986; Graebe, 1987) are species and ecotypes (Heide, 1980, 1989fl), have
compatible with the hypothesis that the SD primary wide temperature and daylength limits for primar\'
induction in dual induction grasses is mediated by a induction as well as a relati\-ely rapid response to
reduction in the level of active gibberellins. in other inductive conditions (small primary induction re-
words, the effect of SD may be to remove the quirement). In such high-latitude grasses, primary
inhibitory effect of LD (and GA) in a way similar to induction requirements are readily met even iti tbe
tbat found in strawberry (Guttridge, 1985). absence of SD at non-freezing temperatures. On the
L^nlike the situation in Loliutn temulentum where other hand, species adapted to low-er latitudes.
GA can substitute for LD, GA^ applied to primary ha\'ing a more strict SD requirement for primary
induced B. inermis plants in SD did not substitute induction, e.g. Bromus inermis (Heide, 1984) will get
for a transition to L D as expected (Heide et al., inadequate primary induction under high-latitude
1987). There is thus no parallel in this SLDP to the conditions as illustrated in Figure 5. These relations
situation in the LSDP Bryophyllum which responds have important implications for localization of
to GA application in SD with normal floral induction commercial grass seed production (Heide, 1980,
and development (Zeevaart, 1985). Nor could GA;, 1990; Aamlid, 1993). In Norway the primary
applied to primary-induced Poa pratensis plants in induction period is often marginal and limiting for
SD with fully differentiated inflorescence primordia seed yield in grasses with predominantly SD in-
substitute for LD and trigger culm elongation and duction (e.g. Bromus inermis and Dactylis glomerata,
inflorescence development (Heide et al., 1987). Heide, 1984, 1987) especially because of the rela-
Although leaf elongation was strongly stimulated, tively high temperature optimum for the SD re-
heading and inflorescence development were not. In sponse. This also appears to be the main reason for
fact, a large proportion of the primordia aborted in very low seed yields of Bromus inermis in Alaska
continuous SD whether GA was applied or not. (Hodgson, 1966; Klebesadel, 1970).
Possible explanations for this unexpected result A further adaptation to the high-latitude en-
might be increased competition between inflores- vironment is tbe initiation of inflorescence primordia
cence and leaf growth due to nutrient diversion to in the autumn among arctic-alpine grasses (e.g.
the GA-sprayed leaves, or that specific gibberellins Hodgson, 1966; Habjorg, 1979; Heide, 1980,
are required for flowering (Pharis et al., 1987). 1989 a). This facilitates early heading and flowering
360 O. M. Heide

flowering and reproduction of temperate perennial


grasses are well adapted to and synchronized witb
the seasonal changes of temperature and daylengtb at
tbe higher latitudes where they grow. The primary
induction requirements are met by tbe decreasing
daylengtb and temperature of autumn and winter,
while the increasing daylength and temperature of
spring and early summer satisfy the secondary
induction requirements. The ability ofthe temperate
grasses to respond to such seasonally determined
environmental signals represents an effective and
crucially important mecbanism for fitting tbeir life
cycles to tbe dramatic seasonal changes of tbe higb-
latitude environment.

ACKNOWLEDGE M E N T S
-5 -
I thank Dr L. T. Evans for his helpful comments on the
6 12 18 24
manuscript and Ms L.-A. Eriksen for typing assistance.
Photoperiod (h)

Figure 5. Climate-photothernis for Troniso (69° 39' N)


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