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Review of Flowering Control in Industrial

Hemp
a a a
Jack Hall , Surya P. Bhattarai & David J. Midmore
a
Centre for Plant and Water Science, Faculty of Science,
Engineering and Health, CQUniversity, Rockhampton, Queensland,
Australia
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ISSN: 1544-0478 print/1544-046X online
DOI: 10.1080/15440478.2012.651848

Review of Flowering Control in

Industrial Hemp

JACK HALL, SURYA P. BHATTARAI, and DAVID J. MIDMORE

Centre for Plant and Water Science, Faculty of Science, Engineering
and Health, CQUniversity, Rockhampton, Queensland, Australia
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Hemp ( Cannabis sativa L.) is a dioecious annual that commences

its reproductive cycle when photoperiods are shorter than a crit-
ical length. Photoperiod-sensitive varieties grown in low latitudes
with short-day lengths tend to produce early flowering, short plants
affecting the yield and quality of the fiber. The photoperiodic sen-
sitivity of the crop could be controlled by the activation or deacti-
vation of genes triggered by the change in light duration perceived
by photoreceptive pigments. The sexual dimorphism of Cannabis
is genetically determined by the XY chromosomal mechanism
although sexual morphology is primarily a result of endogenous
plant growth regulator levels that fluctuate in response to envi-
ronmental variables. Occurrence of occasional hermaphroditic
flowers and monoecious plants are probably the result of these fluc-
tuations. Understanding the mechanisms of photoperiodicity and
sexual inheritance contributes to advances in breeding and crop
management that may underpin the expansion of the commercial
cultivation of the crop in nontraditional agroecological domains.

KEYWORDS industrial hemp, photoperiod, flowering, fiber yield,

crop physiology

INTRODUCTION

Hemp (Cannabis sativa L.) is one of the earliest known cultivated crops
having been for centuries used in textiles, canvas, cordage, paper, and

Address correspondence to Jack Hall, Centre for Plant and Water Science, Faculty of
Science, Engineering and Health, CQUniversity, Rockhampton, Queensland 4702, Australia.
E-mail: j.hall@cqu.edu.au

23
 24 J. Hall et al.

oil. In more recent times, technological advances have expanded the

range of application for the plant and it is now found in geotextiles,
composites, plastics, home insulation, cosmetics, and various other prod-
ucts. As a fiber crop, it has an estimated carbon sequestration rate of
up to 0.67 t/ha according to Pervaiz and Sain (2003). They suggest, for
example, that around 3 t of CO2 emissions could be saved per cubic
meter of thermoplastics, by substituting fiberglass reinforcement for hemp
fiber.
The outer bast (bark) fibers of the stem are recognized as some of
the strongest natural fibers in the world and are the most economically
viable plant component. These are long fibers (10–100 mm) with ten-
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sile strengths ranging from 550 to 900 MPa (Wambua et al. 2003). The
woody core (hurd), consisting of much shorter fibers (>0.5 mm), is used
for pulping, animal bedding, and concreting “hempcrete” (Elfordy et al.
2008).
Hemp cultivation worldwide has been steadily increasing in the past
20 years in response to rising demand for renewable fiber sources and
“clean” agricultural practices. In the years 1989–1998, the area under hemp
production experienced an eightfold increase in the European Union after
the lifting of growing bans in various countries during the 1990s (Bocsa
and Karus 1998). In Australia, hemp fiber production under license has
been adopted although only limited quantities of fiber are produced annu-
ally with no advanced processing facilities in operation. The small scale
of cultivation in Australia is confounded by laws that prohibit the sale of
hemp grain as a human food source, although legislation is under review.
Presently, fiber hemp is a nonviable crop in subtropical Australia due to
lack of suitable low THC (9 tetrahydrocannabinol), late flowering varieties.
The aim of this paper is to explore the mechanisms that control flowering
times and sexual morphology of industrial hemp for the development of
improved breeding and crop management strategies of tropical–subtropical
production.
The mechanisms that control the reproductive responses in Cannabis
sativa L., both industrial hemp and marijuana, have been well documented.
The endogenous genetic and hormonal controllers as well as environmental
factors, e.g., photoperiod, temperature, and stress influence the reproduc-
tive abilities of Cannabis. Sexual expression and flower induction can be
anticipated or controlled by understanding these factors. In many plants,
flowering occurs when the meristematic tissue receives signals produced
by changes in temperature and/or light duration and/or quality (Horvath
2009). The transition to floral induction is a critical time for successful repro-
duction particularly in dioecious species such as Cannabis that rely heavily
on homogenous, synchronized flowering (Amaducci et al. 2008; Bocsa and
Karus 1998). The shift from vegetative growth to flowering is the major
phenological process in hemp plants and extensive studies detailing the
 Flowering Control in Industrial Hemp 25

origins of these processes in various species, such as Arabidopsis thaliana

(Amasino 1996; Ma 1998; Sheldon et al. 2000), have started to uncover
genetic sources of the process, particularly those involved in photoperiodic
response. Understanding the mechanisms that control flowering in industrial
hemp will provide the basis for delineation of specific growing seasons in
suitable regions, as well as underpinning the achievement of maximal crop
yields.

FLOWERING IN HEMP
Reproductive Development of Hemp
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The Cannabis genus originated in Central Asia and eventually diversified

into various landraces and cultivars used for industrial (hemp), medicinal,
and recreational purposes. It is a wind-pollinated, herbaceous, dioecious
annual. Life cycles last between 4 and 6 months (Clarke 1999) but may
be longer or shorter depending on the variables. When grown in opti-
mum light duration and temperature conditions, the vegetative period is
prolonged, ensuring tall stems necessary for fiber production. From the
first appearance of flower primordia, 4–6 weeks pass until full flower-
ing, with male flowers opening a few days before the females. Following
flowering, which lasts 2–3 weeks, male plants senesce having fulfilled repro-
ductive purposes (Bocsa and Karus 1998). Females survive for a further
3–5 weeks while the seed matures. During this period, leaves senesce
as proteins and fats are synthesized in the seeds (Meijer et al. 1995).
In one study, Meijer et al. (1995) found that as a result of this senes-
cence, the radiation use efficiency (RUE) declined from 2.2 to 1.1 g/MJ after
flowering.
Talley (1934) observed that carbon to nitrogen ratios (C:N) of the upper
plant parts also differ between the sexes at flowering. The author con-
ceded that high carbohydrate levels in male plants and higher N levels in
females are simply suggestive of the phenological fate of each sex. Flowering
exhausts male plants that are no longer capable of N assimilation from the
soil while females continue to acquire nutrients during grain-fill.
Prior to the formation of reproductive primordia, although highly dimor-
phic at maturity, the two sexes are indistinguishable. The first signs of
flowering are undifferentiated flower buds forming in the stipules at the
fourth to sixth leaf nodes (Cervantes 2006). Males can eventually be identi-
fied by the pointed buds with five radial segments forming in pairs at petiole
nodes. Female flowers are more inconspicuous and are only identifiable
early by the appearance of dual, fork-shaped stigmas protruding from tubu-
lar bracts. As flowering continues, large inflorescences form on both sexes
with males hanging in large loose, highly branched panicles and female
flowers tightly packed around the leaf axils. Flowers form and mature on
 26 J. Hall et al.

the inflorescence from the bottom to top. At flowering onset, the phyllotaxy
(leaf arrangement) changes from opposite to alternate and, as inflorescence
develops, leaflet sizes gradually decrease until only small, single leaflets are
left below flowers.
Advanced female flowers consist of a single ovary inside a green,
single-leaf bract with visible yellow, white, or pinkish stigmas. Bracts swell
soon after pollination as achene development begins. If left unpollinated,
the stigmas continue to grow and buds produce increasing amounts of
cannabinoid-containing resins from glandular hairs (trichomes). Male flowers
are small, yellow–white, and star-shaped with greenish–yellow anthers pro-
ducing masses of pollen. Fiber hemp is generally harvested at 50% male
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flowering (Bocsa and Karus 1998).

Sexual Phenotypes
Sexual dimorphism in flowering plants is a relatively recent evolutionary
occurrence (Dellaporta and Calderon-Urrea 1993). This adaptation creates
obligatory out-crossing, promoting strong genetic variation within popula-
tions, and reducing the likelihood of inbreeding. Most angiosperms have
hermaphroditic flowers, where male and female organs are present in the
same flower. A smaller group of plants (around 10%) have unisexual flowers
that have vestiges of only a single sex (Thomas and Vince-Prue 1997).
These species may have both female and male flowers on the
same plant (monoecious) or female and male flowers on separate plants

FIGURE 1 Female inflorescence of industrial hemp (color figure available online).

 Flowering Control in Industrial Hemp 27
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FIGURE 2 Male flower bud cluster showing open flowers (color figure available online).

(dioecious). Unisexual hemp populations (predominantly female) are pro-

duced commercially by crossing female plants with monoecious males. The
resulting hybrid is 70%–85% female, 10%–15% monoecious, and 1%–2% male
(Bocsa and Karus 1998).
Dioecious plant species usually produce hermaphroditic flower pri-
mordia that eventually differentiate through reduction or abortion of the
sexual organs that are inconsistent with the internal sexual gearing. In cer-
tain species such as Cannabis, Spinacia, and Murcurralis, flowers develop
true to the genetic sexual orientation and do not generally produce
hermaphroditic flower primordia (Lebel-Hardenack and Grant 1997; Thomas
and Vince-Prue 1997), although hermaphroditic flowers and monoecious
plants do occasionally occur in Cannabis. Dioeciousness in Cannabis
largely occurs with approximately equal ratios of males to females although
under certain conditions this ratio may polarize, usually to favor morpho-
logically feminine (carpellate) individuals (van der Werf and van den Berg
1994). Females are slightly predominant in most hemp crops at a ratio of
107–113 females to every 100 males (Bocsa and Karus 1998). Breeding
strategies and chemical manipulation have the potential of achieving greater
unisexuality in crops. Chemical manipulation can be a costly proposition for
the industry as it has to be applied for each individual crop, hence, breed-
ing and selection for unisexuality is an attractive option to the industry.
Predominantly, male fiber crops may yield higher quality bast fiber com-
pared to a conventional dioecious crop, whereas a greater seed volume can
be produced from a mostly female population.
Monoecious hemp has a typically “female” growth habit but is highly
variable in floral arrangement and flower sex ratios. Despite retaining the
 28 J. Hall et al.
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FIGURE 3 Monoecious hemp panicle with male flower ‘whorl’ below female flowers (color
figure available online).

same flower structures of the dioecious plants, inflorescence formation dif-

fers significantly. The typical monoecious hemp plant produces male flower
clusters in whorls on stem nodes, whereas female flowers are grown at
the tops of branches and above stem nodes. These plants are less prolific
pollinators and produce fewer flowers than dioecious hemp.

DETERMINANTS OF SEXUAL MORPHOLOGY

AND FLOWERING DYNAMICS
Genetic Determination of Sex in Hemp
Sexual expression in Cannabis is largely genetic (Flachowsky et al. 2001;
Mandolino et al. 2002), but can be altered through environmental influences.
Tournois (cited in Thomas and Vince-Prue 1997) was the first to report
sexual reversal in the Cannabaceae family when he observed the effects
of short photoperiods on Hops (Humulus japonicas) and Cannabis. He
noticed a tendency toward maleness in Cannabis despite most dioecious
plants showing a female tendency under similar light conditions.
 Flowering Control in Industrial Hemp 29

Sexual determination in Cannabis is controlled by sex chromosomes

and a number of researchers have described the homo–heterogametic (XY)
system of the genus (Hirata 1924; Moliterni et al. 2004; Rode et al. 2005)
despite its rarity in dioecious species. Isolation of sex-specific genetic mark-
ers in male plants supports the theory of homo–heterozygosity, although no
markers have yet been found in females (Flachowsky et al. 2001; Mandolino
et al. 2002; Sakamoto et al. 2005).
Despite the presence of sex chromosomes in Cannabis, they are
not the sole determining factor of sexual morphology. The prevalence of
monoecious plants and intersexual flowers within Cannabis populations
challenge the notion of simple XY inheritance for controlling the mor-
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phology of all individuals, and suggest that other factors disrupt gender
purity and cause viable male flowers on genetically female plants and vice
versa (Bocsa 1999). Sexual reversal in dioecious plants through hormonal
manipulation demonstrates the bipotency of sexually predetermined plants,
indicating that sex genes control endogenous plant hormones that influence
sexual morphology (Dellaporta and Calderon-Urrea 1993).

Chemical Influences on Flowering Behavior

Plant growth regulators (PGRs) and some chemical agents can modify sexual
expression and morphological responses in plants. Arabidopsis thaliana, a
long-day plant, responds to gibberellic acid (GA) application by inducing
the reproductive phase during shorter days. Plants with defective gibberellin
production tend to flower much later (Amasino 1996). Prat et al. (2008)
observed that GA applied to the dioecious jojoba (Simmondsia chiren-
sis) resulted in a reduction in flower number while cytokinin caused an
increase in floral expression. GA induces male characteristics in Cannabis
while auxins, ethylene, and cytokinins induce the expression of female
traits. Thomas and Vince-Prue (1997) induced femaleness by lowering
endogenous gibberellin levels in male plants using a chemical gibberellin
retardant and by treating plants with morphactins altering the biochemical
auxin/gibberellin ratios.
Cytokinins originating in root material may also promote feminization
as root removal leads to increased masculinization of plants. A study by
Chailakhyan and Khryanin (1978) involving drenching hemp seedling root
systems with various PGRs confirmed the effects on sexual expression. Plants
treated with 15 mg/L of both 6-benzylaminopurine (cytokinin) and indole-
3-acetic acid (auxin) resulted in purely feminine or hermaphroditic plants.
A similar result was observed when plants were treated with abscisic acid
(ABA). Treatments of GA (25 mg) resulted in 80% masculine plants.
Other nonendogenous compounds are used to similar effect. Silver thio-
sulfate (STS) is commonly used in the marijuana industry to produce male
flowers on genetically female plants (Green 2005). Progeny produced from
 30 J. Hall et al.

seed pollinated from these “male” flowers are exclusively female (Ram and
Sett 1982) as, presumably, only feminine (XX) chromosomes are inherited.
The role of chemically altering sexual expression may at present be lim-
ited to controlled activities, such as breeding programs aimed at increasing
seed production (e.g., using STS). Commercial use of certain compounds for
the purpose of achieving unisexuality in hemp, however, may be beneficial
in attaining more productive fiber and grain crops.

Environmental Effects on Flowering

In addition to genetics and chemical influences, flowering is affected by
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the functions of environment, notably temperature and light quality and

quantity. It is widely accepted that cold periods (vernalization) are neces-
sary in species such as Arabidopsis (Reeves and Coupland 2000; Sheldon
et al. 2000), and certain cereal species for phenological transitions such as
flowering to take place (Dennis and Peacock 2007). Cannabis does not
rely on a cold period for any developmental stage but heat may deter-
mine the qualities and timing of the floral stage. Amaducci et al. (2008)
used the combination of temperature and photoperiod to model the poste-
mergent phenology of industrial hemp grown in Italy. This is a necessary
approach, as high temperatures accelerate flowering in hemp by decreasing
the duration between the formation of flower primordia and full flower-
ing whereas cold temperatures prolong it. Besides cold periods, stresses
caused by mechanical damage, nutrient toxicities/deficiencies, and changed
light conditions are responsible for variations in sex ratios in hemp and the
increased likelihood of monoecism (Clarke 1999).
Hemp phenology is also sharply dependant on light quality. In some
species of angiosperm, the intensity of flowering is affected by the amount of
light received before floral induction. This may simply be the requirement
of sufficient photosynthesis for the production of reproductive organs but
in plants such as Xanthium, flowering ceases entirely when given insuffi-
cient light prior to inductive dark periods (Thomas and Vince-Prue 1997).
The inductive dark period may be interrupted with as little as 5 E.m−2 .s in
Cannabis (Lisson et al. 2000).

Photoperiodism in Hemp
The initiation of the flowering process in response to environmental
cues, such as photoperiod and temperature, is an evolutionary mechanism
designed to synchronize reproduction at optimal times (Amasino 1996).
Higher plants may be classified, according to their phenological response to
photoperiod, as short-day, long-day, or day-neutral plants. Short-day plants
(SDPs) require a minimum dark period or “short-day” to trigger the transition
 Flowering Control in Industrial Hemp 31

from the vegetative to reproductive phase. Long-day plants (LDPs) require a

minimum light period for the same process and day-neutral plants are unaf-
fected by day length for reproductive initiation. Some day-length sensitive
species commence the transition only after a single inductive photoperiodic
cycle while others rely on continuous favorable cycles. “Fractal induc-
tion” can occur where nonconsecutive cycles have a cumulative effect
on floral induction and partially induced plants may result from less than
ideal photoperiodic conditions (Thomas and Vince-Prue 1997) implying a
quantitative rather than qualitative response mechanism.
Imaizumi and Kay (2006) described the photoperiodic control mecha-
nism as comprising two components: the circadian clock and a circadian-
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regulated photoperiodic measurement system. The “external coincidence

model” is the most accepted explanation of how photoperiod influences
plant phenology and can be defined as when light perception coincides with
an internal timing system causing a physiological response (Davis 2002).
In this model, light has the role of resetting the circadian rhythm that con-
trols the oscillation of a regulatory constituent. The other role of light is to
control the function of the component that promotes flowering in LDPs and
inhibits flowering in SDPs. The photoperiodic response is triggered when
the regulatory component coincides with the day length. The circadian clock
in plants is generated by an array of different oscillators that maintain the
24 h rhythmic cycles (Samach and Gover 2001). Similarities in the circadian
rhythms have been observed in flowering plants, but certain mechanisms
that control flowering are unique to SDPs (Song et al. 2010).
Photoperiodicity is controlled by several genes responding to photore-
ceptor signals and the circadian clock. The LDP Arabidopsis is used as a
“model” species for the study of photoperiodism in higher plants, particu-
larly the circadian-controlled factors that promote flowering. The “master”
gene CONSTANS (CO) and other transcription factors determine the transi-
tion of Arabidopsis from vegetative to reproductive development (Serrano
et al. 2009). Related genes have been identified in other species such as
the alga (Chlamydomonas reinhardtii), pea (Pisum sativum) (Nilsson 2009),
and SDPs such as rice (Oryza spp.) and morning glories (Pharbitis spp.)
(Samach and Gover 2001). At least four genes have been isolated in peas
that control flowering (Wenden and Rameau 2009). These inhibit vegeta-
tive growth, stimulate/inhibit floral production, or work at the meristem
to induce receptiveness to biochemical signals (Colasanti and Sundaresan
2000).
Light is perceived by the leaves of day-length sensitive plants, thus gen-
erating signals that either promote or anti-inhibit flowering in the shoot apex
(Thomas and Vince-Prue 1997). The term “florigen” is used for the nonde-
script chemical that is transported from leaf to shoot for flower induction.
Although it has not been identified chemically, a protein has been isolated as
a molecular marker for florigen in Arabidopsis (Tsuji et al. 2011). This gene
 32 J. Hall et al.

is expressed when inductive day lengths are perceived in leaf phloem tis-
sue. Studies conducted to determine the velocity of florigen through the
phloem showed that photoperiodically induced leaves caused flowering
when grafted onto noninduced plants. Velocities recorded for the substance
were 2.4–3.5 mm/h (Colasanti and Sundaresan 2000).
When the signal is received by the meristem, progenitor cells that pro-
duce vegetative organs undergo a series of transformative processes and
begin producing floral cells. Exceeding threshold levels of accumulated
floral stimuli may be required for full transition in some species (Thomas
and Vince-Prue 1997). This process is reversible in many species including
Cannabis when the plants are returned to noninductive conditions, which
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is likely the result of transmissible inhibitors released from leaves.

Light is perceived in the leaves of plants through sensitive pigments
(photoreceptors), namely phytochromes and crytochromes. Phytochrome is
the most important photoreceptor in vascular plants (Salisbury and Ross
1992), expressing in two light-absorbing forms, far-red (Pfr) and red (Pr).
Pfr is readily converted into Pr when exposed to Pfr light and Pr light will
convert Pr into Pfr. SDPs may not flower if the critical dark period required
for floral induction is interrupted with a short illumination of Pr light a few
hours after the beginning of the dark period. The process is reversed when
plants are then exposed to short illuminations of Pfr light. The duration of
exposure required for reversal depends on the duration of Pr light exposure.
This process indicates that Pfr light is integral for successful flower induction
in day-length sensitive plants (Amasino 1996).
Various isoforms of phytochrome are responsible for different tasks.
Phytochrome A is the most active in SDPs and promotes flowering in LDPs,
such as Arabidopsis and Pea (Pisum sativum). Phytochrome B and other iso-
forms are probably responsible for delaying flowering time. Cryptochromes
absorb blue-light and long-wave UV light and play an important role in reg-
ulating photoperiodic flowering in species such as Arabidopsis (Ma 1998).
The role of phytochromes and cryptochromes in regulation of photoperiod
and controlling flowering in industrial hemp is not yet investigated in detail
so as to be well understood.

IMPLICATIONS FOR HEMP INDUSTRY

Industrial hemp and marijuana varieties of Cannabis undergo premature

floral transition when exposed to short days less than 14–16 h in length. This
limits the cultivation of hemp to the spring/summer period when daylight
hours are longer. Dark periods must be uninterrupted and usually require
a minimum number of inductive cycles for flowering. Undifferentiated and
unformed flowers may be the result of too few inductive days (Clarke 1999).
Amaducci et al. (2008) divide hemp development into three stages: juvenile
 Flowering Control in Industrial Hemp 33

phase, photoperiod inductive phase, and harvest or 50% open male flowers.
The juvenile and harvest stages are expressed in thermal time as they are
not dependent on photoperiod, whereas the photoperiod inductive phase
is jointly influenced by day length and air temperature. If day lengths are
longer than the critical short-day required, then the photoperiod inductive
phase will be delayed and flowers may or may not eventually form.
Varietal differences in photoperiodic sensitivity are pronounced when
hemp with early flowering characteristics is grown at low latitudes. Northern
European hemp grown in Southern Europe or in subtropical regions, such
as South Africa and Australia, performs poorly due to premature flowering
resulting in shorter vegetative periods that limit stem growth (Amaducci et al.
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2008). Central Russian varieties grown in the lower latitudes of Hungary

will flower within 60 days. The opposite occurs when southern European
varieties are grown in northern regions (Bosca and Karus 1998). A northern
limit to industrial hemp production has been suggested at 64–65◦ N (Pahkala
et al. 2008).
Extending day length also alters the sex proportion of flowering hemp
plants. Trials conducted by van der Werf et al. (1994) concluded that the
number of flowering feminine plants is less influenced by day length than
the number of male plants. Male and monoecious plants failed to flower
when photoperiod was above optimal and overall flower numbers were
reduced in both sexes as photoperiod increased. In contrast, if the crop is
grown under day lengths that are shorter than the critical day length, the
photoperiod inductive phase will be instantaneous and rapid floral develop-
ment will occur as soon as the juvenile phase is complete (Amaducci et al.
2008).
The juvenile phase of photoperiod-sensitive plants is not influenced by
the photoperiod. The length of the phase is determined by two possible sce-
narios: the size of the plant dictates the development of reproductive organs
or the apical meristem is independently timed to produce floral vestiges.
Inductive day lengths were shown to be ineffective in promoting flower
bud formation in juvenile Bryophyllum plants, but when induced adult
leaves were grafted onto the juveniles the plants produced floral shoots
(Thomas and Vince-Prue 1997). It may then be inferred that the leaves of
juvenile plants are biochemically too immature for producing floral signals.
Cannabis, however, may undergo “crisis” flowering if exposed to short days
during the juvenile phase and produce hermaphroditic plants (Green 2005).

CONCLUSIONS

The cultivation of low-THC industrial fiber hemp varieties has rapidly

increased in temperate regions of the northern hemisphere in response to
the demand for renewable fiber sources, yet the photoperiodic requirements
 34 J. Hall et al.

of the crop limits tropical production. Hemp flowers prematurely when

exposed to photoperiods shorter than around 14 h. This limits the grow-
ing season of the crop to the spring/summer period in conventional
cropping systems when suitable day lengths delay flowering. The isola-
tion of photoperiod-controlling genes may assist breeders in developing
delayed-flowering varieties suitable for tropical and subtropical regions.
Cannabis is a dioecious species with occasional monoecious individ-
uals within a population. The breeding of unisexual hemp or the chemical
manipulation of sexual expression of the plants has the potential of increas-
ing yields in both fiber and grain crops. Predominantly, male crops may
provide high-quality fiber and feminized crops produce high grain yields.
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Early applications of PGRs onto newly sown crops would influence crop sex-
ual morphology and growth habit: gibberellins induce maleness in plants,
and ABA induces feminine plants. The feasibility of such a practice on a
large scale requires investigation.

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