Fern Laminar Scales Protect Against Photoinhibition from Excess Light

2006·6.2 MB·English

by  J E Watkins

American Forn Journal 96[3):83-g2 (2006]
Laminar
Fern Scales Protect Against Photoinhibition
from
Excess
Light
1
Watkins,
E.
Jr.
J.
USA
Department FL 32611
University of Florida, of Botany, Gainesville,
Akito Y. Kavvah/vra
MD
University of Maryland, Department of Entomology, CoUogo Park, 20742
Stacy
A. Leicht
CT
University of Connecticut, Department of Ecology and Evolutionary Biology, Storrs, 06269
Auld
Josh R.
PA
Department 15260
University of Pittsburgh, of Biological Sciences, Pittsburgh,
AbRAM
BrCKSLER
J.
University of Department of Natural Resources and Environmental Sciences,
Illinois,
Urbana, 61801
IL
Kristine Kaiser
University of Miami, Department of Biology, Coral Gables, FL 33124
—
The Elaphoglossum paleaceum were studied determine
Abstract. laminar scales of the fern to if
We
they act as a morphological mechanism to protect leaves from excess light. hypothesized that if
scales serve this purpose, then individual plants growing in high light would have greater laminar
scale density than those in low light. For our first experiment, plants from high light roadsides
were collected and subjected to artificial scale removal and then exposed to super-saturating pulse
We
removed
of light for 30 min. found that leaves with their scales exhibited significantly greater
photoinhibition than leaves with scales intact. Leaves with intact scales recovered fully after
twelve hours whereas those with scales removed remained photoinhibited. Scale density on the
was with The data from study
adaxial side of leaves positively correlated light intensity. this
and
indicate that fern laminar scales help redu[:e photoinhibition potentially function as
photodamage.
a morphological defense against
The function of leaf vestiture has long been a hotanical curiosity. Apart from
many
their utility for taxonomic purposes, leaf hairs and scales play roles that
and
Manetas,
influence plant physiology (Karabourniotis, Kyparissis,
directly
Lambers, Chapin and Pons, 1998; Karabourniotis and Bornman, 1999;
1993;
111,
One
and
Manetas, 2003; Liakopoulos, Stavrianakou, Karabourniotis, 2006).
commonly mechanism boundary
cited the modification of leaf layers
is
Chapin and However, can
(Lambers, Pons, 1998]. leaf vestiture also directly
111,
and can
influence physiology related to light alter the internal light
environment and Bornman, and
of a leaf (Karabourniotis 1999), reflect visible,
UV
may
infra-red, or harmful radiation (Manetas, 2003). There also be
important tradeoffs in that while photosynthesis reduced in pubescent
is
leaves relative to glabrous leaves, pubescent leaves are often protected from
^Current address: Department of Organismic and Evolutionary Biology, Harvard University,
MA
Biological Laboratories, 16 Divinity Ave., Cambridge, 02138.
AMERICAN FERN JOURNAL: VOLUME NUMBER
84 96
(2{){)(i)
'A
overheating, excessive water loss [Ehleringcr and Bjorkman, 1978] and the
harmful Pammenler, and
potentially effects of exc:essive light [Ripley, Smith,
Morales Manetas,
1999; 2002; 2003].
et
al.,
Exposure excessive can have negative multiple physiolog-
to light effects
at
When
exposed energy can be
ical levels. a leaf is to light, this transferred to
three pathways: photosynthesis, heat, and fluorescence. While directing
we
energy photosynthesis most pathway
into is the beneficial for plants, will
on
focus flnorcscence in this paper. Plant ph3^siologists use measures of
fluorescence as an indicator of chlorophyll stress specifically in relation
to
when
photosystem Greater fluorescence photosystem
results (PSII]
II. II
damaged
reaction centers are closed or and can no longer accept additional
when
electrons, thus interrupting electron transport. Reaction centers close
which
they receive light in excess of that they can transfer. Plants can dispose
of this excess light energy various biochemical mechanisms. the mechanisms
If
in place to deal with excessive light are inadequate, photosystems can become
damaged damage commonly
(extreme results in the observed bleaching
effect].
Both and photodamage
excess light alone result in Photoinhibition: the decline
Demmig
in photosynthesis due to exposure to excess light (Powles, 1984; et
ciL,
1987; Krause, Virgo, and Winter, 1995; Lambers, Chapin and Pons,
1998].
III, If
damage
to the pholosynthetic machinery has not occurred, photoinhibition
is
easily reversed following short recovery times (hours]. However, photo-
if
damage may Adams
has occurred, photosynthetic recovery take days (Demmig-
and Adams,
1990].
The
ability of species to recover from the effects of stress associated with
high light has been relatively well studied in tropical angiosperms (Mulkey
and Pearcy, 1992; Lovelock, and Osmond, Lovelock
Jebb, 1994; ah, 1998]. In
et
general, species recovery closely correlated with that species' natural
is
distribution. Lovelock et (1994] found that gap-dependent species
ciL re-
covered from high light stress faster than species found in dark understory
A
number how
habitats. of additional studies have demonstrated excess
light,
when
combined
especially with other stresses, directly acts to limit species
(Chazdon, Groom, and Kappcn
distributions 1986; Baker, Long, 1991; qL,
et
Kursar and
1998; Coloy,
1999].
Given the ability of light stress to deprt^ss photosynthesis and to shape
species distributions, is not surprising that species have evolved a myriad of
it
complex morphological and biochemical mechanisms allow them cope
that
to
(Demmig-Adams Adams
with and
These
light stress 1992], include
III,
morphological mechanisms such Bornman, and
as leaf hairs (Karabourniotis,
movement when
Liakoura, 1999], leaf or curling to avoid direct solar radiation
leaves are dry (Lebkuecher and Eickmeier, 1993; Sherwin and Farrant, 1998;
Brighigna qL, 2002] and protective biochemical mechanisms such those
et as
that divert energy into pigment conversion carotenoids and the
(e.g.,
(Demmig-Adams
xanthophyll and Adams, and
cycle] 1996; Tausz, Hietz,
metabolism
Briones, 2001a] or glycolate (Larcher, 2003]
known how
about cope with what mechanisms
Little is ferns excess light or
they posses do Biochemical mechanisms, such xanthophyll-mediated
to so. as
W
ATKINS ET FERN SCALES PROTECT AGAINST PHOTOINHIBITION
AL: 85
energy dissipation, have been tentatively demonstrated in the ptcridophytes
Ca
(Eickmeicr,
common
more
Such
some
in pteridophytes as a direct result of leaf drying. leaf curling
reduces the exposed evaporative surface which results in reduced drying rates.
mbination
exposed
added, and perhaps benefit of leaf curling the reduction of
critical, is
incoming polypodiodes
Pleopeltis
photosynthetic tissue to solar radiation. P.
known
vulgare, and Selaginella lepidophylla have long been to exhibit leaf
Homann,
(Lebkuecher and Eickmeier, 1991; Muslin and 1992;
curling
Lebkuecher and Eickmeier, 1993). In the case of lepidophylla, leaf curling
S,
shown and [Lebkuecher and
been both heat
has specifically limit light stress
to
limit
om
kme
Hawaii
and Goldstein (2001] have also showTi that native tree ferns in exhibit
when high an invasive and
greater photoinhibition subjected to light relative to
more widespread tree fern species. Both of these studies indicate that stress
may
play an important role in shaping species distributions.
One mechanism been examined
has not
potential photoprotective that
may
Laminar
thoroughly in the ferns the presence of laminar scales. scales
is
and damage
rpdiirp lipbt thorehv dficroasinp nhotoinhibition limitine to
pxrfifi.q
We
machinerv. oroDOse two hvDotheses: laminar
ll
mor
paleoceum, density species will increase with increasing
scale in this
2]
we examined on
To hypotheses, the
natural these effects
light. test
remov
We
and laminar
occurring increasing light gradient in scale density.
Methous
Materials and
San
This study was conducted the Cuorici Biological Eield Station in the
at
American
W]
montane
which
poleaceum abun-
fern Elaphoglossum (Elaphoglossaceae) (Fig. la) is
dant along high-light roadsides and in the darker understory around the
subgenus Lepidoglossum
Taxonomically, the species within
station. falls
omm
of the leaf (Fig. ib&c). These scales have no vascular connection to the
damage
and removed with no apparent the
sporophyte are easily to
sporophyte.
m
In the a 100 transect was set up along a naturally occurring light
field,
began exposed roadside and continued though an
gradient that a fully site
at
were
nnnn and Three aeed SDoroDhtves collected
area into the forest. similarlv
m
AMERICAN KERN JOURNAL: VOLUME NUMBER
HR
(2()()B)
:i
Fic. 1. Elapboi^hssum paleaccum. A, Haljil; this intlividual was photographed grovvhig on
around
a roadside; in full sunlight Cuorici Biologic:al Fiold Slalion in Costa Txioa. B. Soale
morphology and density on the adaxial surface and of a typical sun leaf. C] Aljaxial surface, B and
C photographed same
the magnification.
at
m m
from
20 of the nearest individuals every along 100
interval
at 5 light
tlie
gradient. Scale density was quantified under a stereoscope on both the abaxial
mm mm
and x
adaxial surfaces of a 10 10 area from each of three sporophytes.
ANOVA
An
was
run determine were
to there differences in scale density
if
among No
we
the leaves of individual plants. differences were found and
therefore calculated the average abaxial and adaxial densities of each three leaf
set.
. ^ -
WATKINS ET FERN SCALES PROTECT AGAINST PHOTOINHIBITION
AL: 87
To environments, hemispherical photograph was taken
assess light a digital
above each sampled individual Nikon Coolpix 950 camera
v^ith a digital
New
[Melville, York, USA) with a fisheye lens attachment. Photographs were
then analyzed using the computer program Gap Light Analyzer (Frazer
et
al.,
1999) estimate the percentage of transmittance. Regression analysis of
to total
the relationships between percent transmittance and scale density on both leaf
JMP
surfaces was performed using the software package [SAS-
statistical
Institute, 2005).
In order to determine whether scales act as a morphological photoprotective
mechanism, were from high roadside
ten plants field collected light
ml
environments with and placed bags containing 250
roots intact in plastic
Two
two were marked on each
of water for hours. leaves of similar ages plant.
On
one frond, scales were removed using the blunt end of a spatula whereas
scales on the other frond were left intact. To establish a baseline of leaf
we
function on the marked fronds, used an Opti-Sciences modulated
flourometer (OS-500) measure chlorophyll fluorescence. For this measure-
to
we
min which
ment, leaves were placed in the dark for 20 after took an initial
measurement were
dark-adapted chlorophyll fluorescence Plants
of (Fv/F^^).
min The
then exposed to a 30 pulse of light at 2000 |imol/m-^/sec-^. pulse of
w
MR16
was produced by Superline 50 halogen bulbs with dichroic
light
made up dozens
coated reflectors. Dichroic coated reflectors are of of layers of
thin materials that reduce the heat generated from the bulb by reflecting infra-
back and away from specimen.
red light into the reflector the
was
Immediately following exposure, chlorophyll fluorescence (F^/FnJ
this
again measured order determine the degree of inhibition relative the pre-
in to
treatment dark-adapted measurement of Fv/F^. To determine the degree of
recovery following exposure to the light treatment, plants were placed in the
measurement was
dark and another dark adapted taken 12 hr post light
[Fv/FnJ
As had removed
treatment. a control, an additional set of plants their scales
A
two sample was
but did not experience the light stress treatment. t-test
performed to determine there were differences between the initial dark-
if
adapted, post light stress (inhibition) treatment, and the 12 hr post treatment
measurements JMP
using software (SAS-lnstitute, 2005).
Fv/Fni
Measurements chlorophyll fluorescence have been widely used in studies
of
measure the general physiological condition or degree of stress that a plant
to
may methods were
be experiencing. Standard chlorophyll fluorescence
The mentioned
followed in this study. initial dark-adapted values of Fv/Fm
maximal quantum Photosystem
above provide an estimate of the efficiency of
which in healthy, unstressed material universally converges around 0.76-
II,
0.83 (Bjorkman and Demmig, 1987). The degree of photoinhibition from the
treatment was determined by comparison the dark-adapted
light to initial
Although photosynthesis not measured there significant
value. directly, is
is
many
lowered values
correlation across studies to indicate that Fv/Fn^ result in
measurements proxy
lowered photosynthetic Thus, of Fv/F^ serve as a
rates.
Demmig, Chapin and
photosynthesis (Bjorkman and 1987; Lambers,
for
III,
Pons,
1998).
AMERICAN VOLUME NUMBER
JOURNAL;
88
l-'ERN 96 3 (2006)
140
• •
•
120 -
•
100 -
•
•
O
•fi
80 -
O o
O
#
°
60 - O
O
O O
O
O
o
O
40 -
cP
•
o
20 - Abaxic Surface
1
O
Adaxic Surface
1
1 1 1
10 20 30 40 50 60 70
Transmittance
(%)
Tho
Fi(j. 2. rolalionship bot\vi)on natural light transmittance and loaf scale density of
Ehiphoglossiiin puJc.aceum.
Rt:SllI,TS
Regardless was
of light intensity of the habitat, scale density significantly
on away
higher the abaxial (bottom surfaces, from exposin-e] than on the
=
adaxial (top surface, facing exposure] of the leaves (data not shown, 6.631,
t
< we
As
found
p 0.0001). predicted, that adaxial scale density increased with
increasing percent transmittance along our sampled bght The
gradient
(Fig.
2).
was = ^
relationship with
significant a linear regression 0.3843, p 0.0035),
(r^
but exhibited a slightly better with a second order polynomial regression
fit (r^
^ ^
0.409, p 0.0115]. There appeared to be no clear relationship between
=
and
abaxial scale density percent
light (Fig. linear regression, 0.0689,
2; r^ p
=
0.2633].
Initial dark adapted measurements indicated that the leaves were healthy
and not experiencing due
stress to transplantation into plastic bags (Fig 3a,
=
n exposure
10, p 0.421). After to supersaturating light, the leaves with
scales intact exhibited significantly less photoinhibition than plants with the
removed
scales n Following hour
(Fig. 3b, 10, 0.0001). the 12 post stress
p
recovery period, leaves with scales intact exhibited significantly greater
recovery than leaves with the scales removed n
(Fig. 3c, 0.0001).
10, p
was
There no
also significant photoinhibition in control plants with scales
removed
exposed
but not
to light stress (n 10, 0.524).
p
WATKINS ET FERN SCALES PROTECT AGAINST PHOTOINHIBITION 89
AL:
Dark-Adapted
Initial
1.0
A p=0.421
t=0.204,
0.8
0.6
0.4
0.2
0.0
Post Light Stress
-
1.0
p<0.0001
t=12.22,
B
0.8 -
0.6 -
0.4 -
0.2
-
0.0
Recovery
12hr
1.0
0.8 -
0.6 -
0.4 -
0.2 -
0.0
Removed
ntact
Elaphoglossum paleacevm with
Changes in photosystem yield [Fv/FnJ from fronds of
Fig. 3. II
scales intact and with scales experimentally removed. A. Initial 20 min. dark adapted control
umol/m"^/soc"\ Recovery
values. B. Fv/F,„ values after 30 min. exposure to a light level of 2000 C.
A two sample = was performed compute
values of 12 hours post light stress. t-test (n 10) to
Fv/F,i,
differences between leaves with and without scales. Error bars are standard errors.
AMI^RICAN FERN VOLUME NUMBER
90 JOURNAL:
90
(2909]
I]
Discussion
The
data from our suggest novel laminar
stud}^ a rule for fern scales: that
of photoprotection. Plants where the scales were removed had
significantly
lower values high which
F^/Fj-,^ after light stress, indicative of greater
is
compared
photoinhibition, to leaves with scales intact. Additionally, leaves
with
scales intact exhibited shghlly, but not significantly lower values
F^./F^^^
high comparison
after light stress in to the dark-adapted values 3a intact
(Fig.
compared
to Fig, 3b intact values; analysis not shown). The
significantly
reduced
rate of Fv/F^i recovery in leaves where scales have been removed
(Fig. Ic) indicates that these plants likely experienced photodamage. Taken
together, these data indicate that the presence of fern laminar scales in
m
photodamage when
that occur plants are exposed excess
to
light.
This hypothesis supported by
is finthcr the positive relationship of scale
density with natural Adaxial was
light intensity. scale density positively
correlated witli an individual plant's natural regime where high
light plants in
had
light greater scale density that plants in low This follows our prediction
light.
that if laminar scales act as a morphological photoprotective mechanism then
plants in high light habitats should exhibit greater investment such
in structures.
Ekiphoglossum
paleaceiim
additionally
intriguing
is in that exhibits leaf
it
curling dining times extreme drought The
of
(pers. obs.). differential pattern of
scale density between the abaxial and adaxial surfaces combined with
leaf
may
curling be explained
morphological
as a last line of defense in times of
drought. During upwards
leaf curling, the abaxial surface curls forming lube
a
that completely hides the adaxial smface This mechanism
(pers. obs.].
more
presents the densely covered abaxial surface exposure incoming
to full
solar radiation. This curling can reduce exposure and slow
surface cvapo-
and
transpiration thus potentially reduce or eliminate the damaging of
effects
extreme
In times of high without drought with
light. light or limited drought,
may
adaxial scale density be sufficient protect the plant from extreme
to
photoinhibition and photodamage. The
interaction of scale density with
light
may
intensity suggests that variation in this character be driven by and
light
some
provides
adaptive
value.
There numerous
are other species of Ekiphoglossum in the flora of this
region that lack scales and leaf curling, yet grow alongside Ekiphoglossum
pakaceum.
among
It is likely that different strategics have evolved these
species with the glabrous taxa relying on biochemical mechanisms. Futme
studies w^ould benefit greatly from inclusion of these species and from
investigation of protective pigments.
ACKNCnVLLUtJMl-NTS
This study was done during the Tropical Ecology courso taught uuder the auspices of the
Orgaiuzatiou for Tropical Studiiis (OTS 04-01). The c;ourse was supportinl by a grant to OTS frojn
We
Andrew W.
Ihe Mellon Foundation. thank Robbin Moran, Chad Piushv, and Crace CrumuKM'
for
on
connni^uts an earlier version of manuscript.
thi;
WATKINS
ET FERN SCALES PROTECT ACAINST PHOTOINHIBITION
AL:
91
Literv\ti:re Cited
BjORKMAN, O. and B. Demmig. 1987. Photon yield of 0-2 ovolntion and chlorophyll fluorescence
among
77-K
charactGristics at vascular plants of diverse origins. Planta 170:489-504.
and and
Bkighicna, L., a. Bennici, C. Tanj G. Tant. 2002. Structural ultrastructural characterization
of SelagirwUa lepidopbylla, a desiccation-tolerant plant, during the rehydration process.
Flora 197:81-91.
Chazdon, R. L. 1986. Light variation and carbon gain in rain forest understory palms. Ecol.
J.
74:995-1012.
Demmig-Adams, and W. W. Adams and
B. 1992. Photoprote[:tion other responses of plants high
III. to
MuL
Ann.
light stress. Rev. Plant Physiol. Plant Biol. 43:599-626.
Demmig-Adams, B. and W. W. Adams. 199C. The role of xanthophyll cycle carotenoids in the
protection of photosynthesis. Trends Plant 1:21-26.
in Sci.
Demmig, B., K. Winter, A. Kruckk and F. C. Czygan. 1987. Photoinhibition and zeaxanthin formation
in intact leaves - a possible role of the xanthophyll cycle in the dissipation of excess light
energy. Plant Physiol. 84:218-224.
DxTRAMD, L. Z. and G. Goldsil'in. 2001. Photosyntliesis, photoinhibition, and nitrogen use efficiency
and
in native invasive tree ferns in Hawaii. Occologia 126:345-354.
Ehleringer, R, and O. Bjorkman. 1978. Pubescence and leaf spectral charac:teristics in a desert
J.
shrub, Encella farinosa. Oecologia 36:151-162.
C.
EicKMEiER, VV. C. Casper and C. B. Osmond. 1993. Chlorophyll fluorescence in the resurrection
plant Solaginella lepidophyUa (Hook & Grev) Spring during high-light and desiccation
stress,
and evidence for zeaxanthin-associated photoprotection. Planta 189:30-38.
Frazer, G. W., C. D. Canham, P. Sallavvay and D. Marinakts. 1999. Gap Light Analyzer. Simon Eraser
University & Institute for Ecosystem Studies, Burnaby, British Columbia, Canada &
New
Millbrook, York.
Groom, Q. N. R. Baker and S. P. Long. 1991. Photoinhibition of Holly [Ilex aquifolium] in the
J.,
Field During the Winter. Physiol Plantarum 83:585-590.
Zone
HoLDRiDGE, L. R. 1967. Life Ecology. Tropical Science Center, San Jose, Costa Rica.
Kappen, L., B. Sciiroeter, T. G. A. Green and R. D. Ski-pelt. 1998. Chlorophyll a fluorescence and C02
exchange of Umbilicarin aprina under extreme light stress in the cold. Oecologia
113:325-331.
KARABOURNicrris, G. and F. Bornman. 1999. Penetration of lJV-y\. UV-B and blue light through the
J.
leaf trichome layers of two xeromorphic: plants, olive and oak, measured by optical fibre
microprobes. Plantarum 105:655-601.
Physiol.
KARABOURNirrns, G., A. Kyparissis and Y. Manei'as. 1993. Leaf hairs of Olea europaea protect
underlying tissues against ultraviolet-B radiation damage. Environ. Ex. Bot. 33:341-345.
KARABOURNifms, BoRNMAN and
G., F. V. LiAKoiRA. 1999. Different leaf surface characteristics of
J.
three grape cultivars affect leaf optical properties as measured with fibre optics: possible
implication in stress tolerance. Aus. Plant Physiol. 26:47-53.
}.
Krause, G. H., a. Virgo and K. Winter. 1995. Higb susceptibility photoinhibition of young leaves
to
of tropical forest trees. Planta 197:583-591.
KuRSAR, T. A. and P. D. Coley. 1999. Contrasting modes of light ac;climation in two species of the
rainforest understory. Oecologia 121:489-498.
New
Lambers, H., F. S. Chapin TIT and T. L. Pons. 1998. Plant Physiological Ecology'. Springer- Verlag,
York.
W. and
Larcher, 2003. Physiological Plant Ecology, Ecopiiysiology Stress Pliysiology Functional
of
4"
Groups, edition. Springer- Verlag, Berlin.
Lebkuecher, G. and W. G. Eic^kmeier. 1991. Reduced photoinhibition with stem curling in the
J.
resurrection plant Selaginella-Lepidophylla. Oecologia 88:597-604.
and W.
LEtiKUECHER, G. G. Eickmefer. 1993. Physiological benefits of stem curling for resurrection
J.
plants in the field. Ecology 74:1073-1080.
LiAKOPOULOS, G., S. Stavrianakou and G. Karabourniotis. 2006. Trichome layers versus dehaired
lamina of Olea europaea leaves: differences in flavonoid distribution, UV-absorbing capacity,
and wax yield. Environ. Ex. Bot. 55:294-304.
VOLUME NUMBER
AMERICAN FERN JOURNAL:
92 96 3 (2006]
mmvery
Lovi-i.ncK, C. E., M. Jebb and C. B. Osmonii. 1994. Photoinliibition and in tropical plant
response disturbance. Oocologia 97:297-307.
spot:i(\s tn
-
LuvLiLOCK, C. E., T. A. KiiRSAR, D. Skillman and K. Winikk. 1998. Photoinhibition in tropical forest
J.
understory species with short- and long-Hvod leaves. Fund. EcoL 12;v^>53-5r)().
Manetas, Y, 2003. The of being hairy: the adverse effects of hair removal on stem
ini[K":)rtanc:o
New
UV-B
photosyntliesis of Vf^rbascum speciosum art! due to solar radiation. Phytologist
158:503-508.
McjKALES, E., A. Abadia, Abadia, G. Montserkat and E. Uil-Pelegrin. 2002. Trit:bonu;s and
J.
photosynthetic pigment composition changes: responses of Quarcus ilax snbsp. ballotu
Samp, and Mediterranean
(Desf.) Qiie^rciis cocciforn L. to stress [:onditions. Trees-Struct.
Fnnct. 16:504-510.
MuLKEY, S. S. and R. W. Pearcy. 1992. hitc^ractions between acclimation and photoinhibition of
photosynth{\sis of a tropical forest understory herb, Alocasia macrorvhizcu during simulated
canopy gap formation. Funr:!, Ecol. 6:719-729.
Muslin, E. and P. Homann. 1992. Light as a hazard for the desiccation-resistant "r(\surrection" fern
Polypodium polypoidos Phmt Cell and Environ, 81-89.
L.
By Annu.
PowLES, S. B. 1984. Photoinhibition of Photosynthesis hidut^ed Visible-Lij^ht. Rev. Plant
Physiol. Plant Mol. Biol. 35:15-44.
Rii'LEv, B. S., N. W. PammI'Nier and V. R. Smicii. 1999. Function of leaf hairs rcjvisited: The hair layer
on leaves Avciolbcca populifolia reduces photoinliibition, but leads to higher leaf
temperatur(\s caused by lower transpiration Phmt 155:78—85.
rates. Phv'siol.
J.
JMP SAS
SAS-histitule. 2005. User's Guide, Institute, hic, Gary.
W. and M. mechanisms
Sni-:R\viN. H. Farran't. 1998. Prottuition against excess light in the
J.
and Xeropby^a Growth
resun"(u:tion plants Craterostigmci wilinsii viscosa. Plant Regul,
J.
203-210.
and The and
Tausz, M., p. Hietz Briones. 2001. significance of carotenoids tocophcM'ols in
CJ.
photoprotection of seven epiphytic fern species of a Mexican cloud Aus. Plant
forest.
].
28:775-783.
Physiol.