Botanical Studies (2009) 50: 171-179.
*
Corresponding author. E-mail: zhaochm@lzu.edu.cn; Fax:
+86-931-8912823; Tel: +86-931-8914305.
INTRODUCTION
Natural hybridization commonly occurs in various
plants, and appears to play a crucial role in plant
variation, speciation and evolution (Grant, 1981). As
well as the common occurrence of alloploidization
through hybridization followed by speciation, evidence
of homoploid recombination speciation has also been
detected in a few plant species (Rieseberg, 1997). Such
Physiological performances of maternally-dependent
genotypes in the homoploid hybrid species Hippophae
goniocarpa
Fei MA, Li-Tong CHEN, Bu-Qing YAO, and Chang-Ming ZHAO*
Key Laboratory of Arid and Grassland Ecology, Ministry of Education, School of Life Sciences, Lanzhou University,
Lanzhou 730000, P.R. China
(Received April 29, 2008; Accepted October 3, 2008)
ABSTRACT.
Most homoploid hybrid species have different maternal donors and these maternal genotypes
usually have biased distributions. It has been postulated that the geographical distributions of these
genotypes may be due to random genetic drift and founder effects following range expansion after the initial
recombination(s) that led to their speciation. However, the preferred habitats in their distributions also suggest
that they may be adapted to different environments, but we have little knowledge regarding their physiological
performances in the same habitats after their initial recombinant speciation when occurring sympatrically.
Hippophae goniocarpa is a newly-evolved diploid shrub species that appears to have arisen via recombination
events between H. rhanmoides ssp. sinensis ¡Ñ H. neurocarp. We compared the physiological performances of
two genotypes with different maternal origins (H. goniocarpa-R and H. goniocarpa-N, mothered respectively
by H. rhanmoides ssp. sinensis and H. neurocarpa) and the two parental species by measuring their: rates
of photosynthesis (A
max
), transpiration (E), quantum efficiencies (QE), carboxylation efficiency (CE), Light
Compensation Point (LCP), instantaneous (A
max
/E) and long-term (£_
13
C) indices of water use efficiency (WUE),
effective quantum yield of PSII (.
PSII
), non-photochemical quenching (NPQ), nitrogen contents per unit
mass and area (N
mass
and N
area
, respectively), mean single leaf area (MSLA), leaf mass per unit area (LMA)
and carbon concentration (C). The two H. goniocarpa genotypes distinctly differed in A
max
, A
max
/E, QE, CE,
NPQ, LCP, long-term WUE (£_
13
C), N
area
, MSLA, LMA and C. In addition, H. goniocarpa-R outperformed
both parental species in A
max
, long-term WUE (£_
13
C), NPQ, MSLA and LCP. However, A
max
and long-term
WUE (£_
13
C) values of H. goniocarpa-N were intermediate between those of the two parental species, and the
variations in these traits showed no correlation with those of the maternal species. The instantaneous WUE
(A
max
/E) and N
area
of both H. goniocarpa genotypes were distinctly higher than those of the two parental
species, further suggesting that this recombinant species may be concordantly transgressive in these respects.
These consistent performance may provide partly inherent power to combine all individuals of two genotypes
as a distinct species unit. In contrast, the MSLA and N
mass
of the two genotypes were intermediate between
those of their parental species and their C concentrations and QE were distinctly lower. Our results reveal
differences in the physiological performances of two genotypes of the same hybrid species with different
maternal donors. These findings should help extend our understanding of the habitat preferences of the
maternal genotypes within a few hybrid species.
Keywords: Genotypes; Hippophae goniocarpa; Homoploid hybrid; Physiological performance.
recombination speciation is completed by reproductive
isolation from the two parental species due to ecological
divergence or chromosomal rearrangements following the
initial homoploid hybridization (Arnold, 1997; Buerkle
et al., 2000). It is possible that both parental species may
serve as maternal donors in such a speciation (Arnold,
1997) and this possibility has been confirmed for most
diploid hybrid species examined to date ¡V including Pinus
densata, Argyranthemum sundingii, Helianthus anomalus
and H. deserticola (Brochman et al., 2000; Wang et
al., 2001; Schwarzbach and Rieseberg, 2002; Gross et
al., 2003). An interesting finding of the cited studies is
PhySIOlOgy
pg_0002
172
Botanical Studies, Vol. 50, 2009
that different maternal genotypes of the same species
usually have different distributions and occupy different
habitats. It has been suggested that the differences in the
distribution patterns of maternal genotypes may be due
to random genetic drift, range expansion and founder
effects following the initial recombination speciation
events (Arnold, 1997). However, it remains unknown
whether these differences in distribution mirror habitat
preferences of maternal-dependent genotypes associated
with differences in their physiological performance.
A recombinant species initially arises from random
hybridization between two parental species (Rieseberg,
1997). The initial hybrids often vary in performance
relative to their parental species, for instance the first
hybrid generation may be heterotic, while hybrid
transgression may be reduced in subsequent generations
(Arnold, 1997; Arntz et al., 1998; Burke and Arnold,
2001; Campbell and Waser, 2001; Johnseon et al., 2001;
Campbell et al., 2005). However, whether or not hybrid
transgression
has played a critical role during their
speciation and mature hybrid species have continued to
be transgressive are questions that have long been debated
(Schemske, 2000). The possibility that recombinant
species have transgressive
performance has been tested
recently (Rieseberg et al., 2003). However, little research
has focused on possible differences in hybrid performance
related to the maternal origins of representatives of natural
homoploid hybrid species. The reproductive isolation of
these hybrid species presumably evolved as a consequence
of divergent natural selection via adaptation to different
niches to those of the parental species (Schluter, 2000).
Therefore, sound knowledge of the physiological
performances of different maternal genotypes in hybrid
species could substantially enhance our understanding
of homoploid speciation mechanisms and the habitat
preferences of the hybrids.
Hippophae goniocarpa was first described from a few
specimens originating from Qinghai and Sichuan, China
(Lian et al., 1995). Individuals of this shrub species vary in
height from 0.5 m to 3 m in the field. Most morphological
characters of H. goniocarpa are intermediate between
those of H. rhanmoides ssp. sinensis and H. neurocarpa.
All H . goniocarpa individuals examined to date are
diploids with 2n = 24 (Lian et al., 1998). These three
species, and others in this genus, are dioecious, wind-
pollinated, and their gender is genetically determined
(Bartish et al., 2000). The hybrid origin of H. goniocarpa
from H. rhanmoides ssp. sinensis ¡Ñ H. neurocarpa has
been unequivocally demonstrated by RAPD and ITS data
(Bartish et al., 2000; Sun et al., 2003). Bartish et al. (2002)
further demonstrated that cpDNA is maternally inherited in
Hippophae and a recent population analysis of these three
sympatric species suggested that both H. rhanmoides ssp.
sinensis and H. neurocarpa had served as maternal donors
to the genetic composition of H. goniocarpa (Wang et al.,
2008). The three species occur in the same habitats in the
northeast Qinghai-Tibetan Plateau in China. However, H.
goniocarpa shows distinct reproductive isolation from H.
rhanmoides ssp. sinensis and H. neurocarpa (Lian et al.,
2000; Wang et al., 2008), and the seed germination and
growth rates of this hybrid species are higher than those
of both parental species. In addition, chromosome pairing
and segregation at meiosis are normal in this species and
it produces highly viable progeny, suggesting that these
individuals represent an independent lineage, rather than
the early hybrid generations (for example, F
1
and F
2
, in
which chromosome pairing and segregation are irregular)
recurrently produced between two parental species (Lian
et al., 2000). All these lines of evidence suggest that
this species has escaped from unfit recombinants (for
example, hybrid sterility and breakdown) from the initial
hybrid generations and completed reproductive isolation.
However, its limited distribution suggests that this species
has not inhabited a different niche from either parental
species through range expansion as in other diploid
recombination species. Therefore, H. goniocarpa provides
a good model system to compare the physiological
performances of different maternal genotypes relative to
its two parental species.
Photosynthesis rates (A
max
), transpiration (E),
instantaneous (A
max
/E) and long-term (£_
13
C) indices of
water use efficiency (WUE), effective quantum yield of
PSII (.
PSII
) and non-photochemical quenching (NPQ),
Light Compensation Point (LCP), nitrogen contents per
unit mass and area (N
mass
and N
area
, respectively), mean
single leaf area (MSLA), leaf mass per unit area (LMA)
and carbon concentration (C) are leaf traits that play key
roles in the physiological performance
of plants (Genty
et al., 1989; Bilger and Bjorkman, 1990; Ackerly, 2004).
LMA strongly reflects the dry-mass cost of producing
new leaves, and correlates negatively with leaf N
concentrations (Wright et al., 2005). Leaf N concentration
is also strongly positively correlated with photosynthetic
capacity (Reich, 2004) because N is essential for the
synthesis of Rubisco, the key photosynthetic enzyme
(Taiz and Zeiger, 1998). In this study, we evaluated
these physiological parameters in two different maternal
genotypes of H. goniocarpo (mothered respectively by H.
neurocarpa and H. rhamnoides) and both parental species.
Specifically, we aimed to address the following questions:
(1) Do the recombinant hybrid species perform differently
from their parents in these physiological respects. (2) Are
there distinct differences between the two genotypes with
different maternal origins.
MATERIAlS AND METhODS
Study site and samples of individuals
We conducted our experiments in the northeast
Qinghai-Tibetan Plateau (38¢X05¡¦ N, 100¢X19¡¦ E; altitude,
2,751 m) where the three species occur sympatrically. A
preliminary analysis of H. neurocarpa and H. rhanmoides
ssp. sinensis (27 individuals of each species) showed that
the chloroplast DNA trnL-F region differs at 15 sites in
pg_0003
MA et al. ¡X Maternally-dependent physiological performances of
Hippophae goniocarpa
173
these two species. Therefore, we analyzed the sequences
of the maternally-inherited cpDNA in this region to
determine the maternal origins of 12 H . goniocarpa
individuals, three of which were found to be mothered by
H. neurocarpa (H. goniocarpa-N) and the other nine by H.
rhanmoides ssp. sinensis (H. goniocarpa-R) (Wang et al.,
2008). We also analyzed the nuclear internal transcribed
spacer region (ITS) to confirm the hybrid origin of all
12 of the H. goniocarpa individuals. The two parental
species differ from each other at nine sites in the analyzed
region of this marker, and none of the sampled individuals
of either H. neurocarpa or H. rhanmoides ssp. sinensis
showed additivity at any of these sites (Wang et al., 2008).
However, all 12 sampled individuals of H. goniocarpa
showed hybrid additivity. We chose four genotypes (H.
goniocarpa-R, H . goniocarpa-N, H . neurocarpa and
H . rhanmoides ssp. sinensis) to conduct the following
experiments and each genotype was represented by three
individuals. The selected individuals had similar heights
around 2.8 m (and thus ages) and are situated in the same
valley.
gas exchange measurements
Photosynthetic parameters were measured using
an LI-COR 6400 infrared gas-analyzer (IRGA; LI-
COR Lincoln, NE, USA) in sunny days, from 09:00 to
11:00 between 12 and 16, August 2005. Five fully and
expanded leaves were selected from the top of the second-
year branches for measurements. Each of the sampled
leaves was individually placed in the leaf chamber of
the IRGA and illuminated by an LI-6400-02B LED
light source (LI-COR) attached to the sensor head. A
range of photosynthetic photon flux densities (PPFD)
between 0 and 2000 £gmol m
-2
s
-1
were used for light curve
measurements, starting at 2000 £gmol m
-2
s
-1
and ending
at 0 £gmol m
-2
s
-1
. During the gas-exchange measurements
the ambient CO
2
concentration in the chamber was
maintained at 360 £gmol mol
-1
, using the LI-6400-01 CO
2
mixture (LI-COR), and leaf temperature was maintained
at 28 ¡Ó 0.5¢XC. The relationship between net assimilation
rate and the intercellular CO
2
concentrations (A-ci curve)
was examined by measuring CO
2
uptake over a range of
external CO
2
concentrations (Ca) from approximately
50 £gmol mol
-1
to 2000 £gmol mol
-1
. Measurements
were taken under saturating light of 1500 £gmol m
-2
s
-1
,
cuvette temperatures were maintained at ambient levels,
and before the measurements each sampled leaf was
illuminated for a few minutes. After measuring leaf area
with a LI-COR-3000A planimeter (LI-COR Lincoln, NE,
USA), values per unit leaf area were calculated for each of
the photosynthetic parameters.
Chlorophyll fluorescence measurements
Chlorophyll fluorescence was measured using a
LI-6400-40 (LI-COR Lincoln, NE, USA) fluorescence
attachment after allowing the leaves to adapt to the dark
for approximately 30 min. The minimal fluorescence yield
(F
o
) and maximal fluorescence yield (F
m
) were measured.
At each PPFD level, the fluorescence yield at steady state
(F
s
) and maximum fluorescence yield in light-adapted
state (Fm¡¬) were respectively determined. During these
measurements leaf temperature was maintained at 28¡Ó
0.5¢XC. The maximum photochemical efficiency of PSII
(F
v
/F
m
), effective quantum yield of PSII (.
PSII
) and non-
photochemical quenching (NPQ) were calculated as
described by Genty et al. (1989) and Bilger and Bjorkman
(1990).
leaf carbon isotope composition and elemental
content
Fifteen leaves of each individual tree were selected to
determine their single leaf area (MSLA) using the LI-COR
3000A planimeter. They were randomly classified into
three groups, then oven-dried for 48 h at 80¢XC, weighed to
determine their LMA (leaf mass per unit area), and finally
grounded using a mortar into fine powders. The powders
obtained from each group were split into two portions.
The isotope composition of one portion of each of the
samples was measured according to Tieszen (1979) using a
MAT-252 (Finnigan, USA) mass spectrometer. The overall
precision in £_-values was better than 0.1. as determined
by analysis of repeated samples. The other portions were
used to determine leaf nitrogen (N
mass
) and carbon (C)
contents using a CHN analyzer (Vario EL, Elementar
corporation, Germany). Leaf N content per unit area (N
area
)
was then calculated by multiplying N
mass
by LMA.
Statistical analysis
One-way ANOVA and Post hoc-LSD tests were used to
compare the physiological parameters between different
genotypes. Prior to comparison, all the data were tested
for normality. We followed Schwarzbach et al. (2001) to
describe whether the measured variables are transgres-
sive (negative or positive) (the hybrid species differed
significantly from parental species) or intermediate (H.
neurocarpa-like or H. rhanmoides-like). Data analyses
were performed and figures were generated using SPSS
software ver. 11.0. Data are presented as means ¡Ó SD.
RESUlTS
Photosynthetic parameters
The light response curves obtained from the four
genotypes were similar (Figure 1a), but their light
saturation levels distinctly differed, being approximately
400-800 £gmol m
-2
s
-1
for H. rhanmoides ssp. sinensis and
H. goniocarpa-N, 800-1000 £gmol m
-2
s
-1
for H. neurocarpa
and 1200 £gmol m
-2
s
-1
for H . goniocarpo-R. The
instantaneous WUE (A
max
/E) values for H. goniocarpo-R
and H . goniocarpo-N also significantly differed, but
were significantly higher in both cases than those of both
of the two parental species (Table 1). In contrast, the
quantum efficiencies (QE) of the two hybrid genotypes
were significantly different, but were lower than those
pg_0004
174
Botanical Studies, Vol. 50, 2009
of the two parental species. The carboxylation efficiency
(CE) of goniocarpa-R was distinctly different from that of
H. goniocarpa-N, and the former genotype had a higher
CE than the two parental species while the latter was
intermediate between the parental species in this respect.
In addition, the light compensation point (LCP) was higher
in H. goniocarpa-R than in the two parental species, while
that of H. goniocarpa-N was lower (Table 1).
Chlorophyll fluorescence
The electron transport rate (ETR) and effective PSII
quantum yield (.
PS
¢º
) increased with PPFDs, and there
were no significant differences in these variables among
the four genotypes (Figure 1b, d). However, their non-
photochemical quenching (NPQ) responses to increases
in PPFDs varied strongly, reaching higher levels in H .
goniocarpa-R and lower levels in H. goniocarpo-N than
in either of the parental types (Figure 1c). In addition,
there was no indication that these differences were due to
significant stressors prior to the measurements because
F
v
/F
m
remained constant, between 0.82 and 0.84.
Carbon isotope ratio and elemental analyses
The long-term (£_
13
C) indices of water use efficiency
(WUE) varied among the four types. ANOVA tests
suggested that H. goniocarpa-R significantly differed
from H . goniocarpa-N in this respect, and the WUE
value was higher for the former genotype than for both of
the parental species while that of the latter was between
intermediate those of the two parental species.
Figure 1. Variance of photosynthetic and chlorophyll fluorescence parameters with increasing light intensities measured in four
genotypes: A (H. neurocarpa), B (H. goniocarpa-N), C (H. goniocarpa-R), D (H. rhanmoides ssp. sinensis). Means ¡Ó SD. a, Net
carbon accumulation (A
n
); b, Electron transport rate (ETR); c, Non-photochemical quenching (NPQ); d, Effective PSII quantum yield
(.
PS
¢º
).
Table 1. Values of photosynthetic parameters derived from light curve and A-ci curve determinations: maximum photosynthetic
rate (A
max
), transpiration (E), quantum efficiency (QE), carboxylation efficiency (CE), instantaneous (A
max
/E), light compensation
point (LCP). Different letters in each column indicate statistically significant differences (P < 0.05) according to one way variance
analysis (ANOVA). Arithmetic means ¡Ó SD.
H. neurocarpa
H. goniocarpa
H. rhanmoides ssp. sinensis
H. goniocarpa-N
H. goniocarpa-R
A
max
(£gmol CO
2
m
-2
s
-1
) 12.5
¡Ó 0.15
a
11.1 ¡Ó 0.22
b
12.8 ¡Ó 0.12
c
8.45 ¡Ó 0.43
d
E (mmol H
2
O m
-2
s
-1
)
3.50 ¡Ó 0.13
a
2.41
¡Ó 0.21
b
2.40
¡Ó 0.18
b
3.71
¡Ó 0.15
c
A
max
/E
3.57 ¡Ó 0.14
a
4.61 ¡Ó 0.22
b
5.34 ¡Ó 0.15
c
2.28 ¡Ó 0.29
d
QE
0.05 ¡Ó 0.006
a
0.0297 ¡Ó 0.0051
b
0.0165 ¡Ó 0.0032
c
0.0322 ¡Ó 0.0047
d
CE
0.132 ¡Ó 0.021
a
0.237 ¡Ó 0.015
b
0.088 ¡Ó 0.011
c
0.071 ¡Ó 0.034
c
LCP
129 ¡Ó 5.2
a
67 ¡Ó 6.9
b
210 ¡Ó 9.4
c
140 ¡Ó 8.2
d
pg_0005
MA et al. ¡X Maternally-dependent physiological performances of
Hippophae goniocarpa
175
There was no significant difference in leaf N
concentrations between H . goniocarpa-R and H.
goniocarpa-N, and both had values between those of the
two parental species. However, leaf C concentrations of
these two genotypes were distinctly different and lower, in
both cases, than those of the two parental species (Figure
2). Furthermore, the two goniocarpa types differed from
each other in N
area
,
and both had higher N
area
values than
the two parental species. The LMAs of the two hybrid
genotypes also differed, but the H. goniocarpa-N LMA
was similar to that of H. rhanmoides ssp. sinensis while
the LMA of H. goniocarpa-R was intermediate between
those of the two parental species. MSLAs of both hybrid
genotypes differed from each other and were intermediate
between those of the two parental species (Table 2).
Compared with two parental species, a few measured
variables in H . goniocarpa and two genotypes are
transgressive or intermediate (Table 3).
DISCUSSION
Physiological performances of H. goniocarpa
Hybridization has played an important role in enhancing
adaptive fitness through complementary recombination,
and heterosis has often been observed in F
1
hybrids
(Arnold, 1997; Campbell et al., 2005). However, such
superiority may be transient and subsequently disappear
in natural recombinant species (Schemske, 2000). Our
physiological measurements suggest that both maternal
genotypes of H. goniocarpa have significantly higher
water use efficiency (WUE, A
max
/E), and nitrogen contents
(N
area
); i.e. both of them are positively transgressive
than their two parental species (Table 3). In addition, H.
neurocarpa tended to have higher water use efficiency
than H. rhanmoides ssp. sinensis, which is consistent with
the habitat distribution of these two species (the former
occurring in a drier region at higher altitudes than the
latter; Lian et al., 2000). This finding is consistent with the
reported heterosis of Ipomopsis F
1
hybrids in instantaneous
water use efficiency (Campbell et al., 2005). However,
to our knowledge, there have been no previous detailed
comparisons of the instantaneous WUE between natural
hybrid species and their parental species. It remains
unknown whether this performance is stable when the
hybrid species extends to the other habitats. However,
the positively transgressive WUE of H . goniocarpa
Table 2. Nitrogen content per unit area (N
area
), leaf mass per unit area (LMA) and mean single leaf area (MSLA) (means ¡Ó SD) in
H. neurocarpa, H. goniocarpo-N, H. goniocarpo-R, H. rhamnoides. Different letters in each column indicate statistically significant
differences (P < 0.05) according to one way variance analysis (ANOVA).
H. neurocarpa
H. goniocarpa
H. rhanmoides ssp. sinensis
H. goniocarpa-N
H. goniocarpa-R
N
area
(g/m
2
)
3.06¡Ó0.27
a
3.93 ¡Ó 0.31
b
3.63 ¡Ó 0.10
c
2.82 ¡Ó 0.08
d
LMA (g/m
2
)
73.44¡Ó6.48
a
101.41 ¡Ó 8.12
b
77.11 ¡Ó 2.25
a
95.59 ¡Ó 2.54
b
MSLA (cm
2
)
1.17¡Ó0.15
a
1.94 ¡Ó 0.11
b
2.37 ¡Ó 0.04
c
2.96 ¡Ó 0.15
d
Figure 2. Concentration of nitrogen and carbon (N%, C%) and
integrated water use efficiency (£_
13
C) measurem ents for the
four genotypes A (H. neurocarpa), B (H. goniocarpa-N), C (H.
goniocarpa-R), D (H. rhanmoides ssp. sinensis) at the study site.
Means ¡Ó SD. Different letters (a, b, c, d) within the same column
denote significant differences (p < 0.05).
pg_0006
176
Botanical Studies, Vol. 50, 2009
may suggest that this physiological performance may be
involved in speciation and ecological isolation of such
recombination species
.
If so, this finding conflicts with
the previous hypothesis that WUE heterosis may not be
genetically based and may be solely due to dominance,
overdominance, or positive epistastis, in which specific
interactions between genes from the two species increase
the trait value in the F
1
hybrids (Campbell et al., 2005).
However, all confirmed homoploid hybrid species have
been found in more extreme habitats than those of any
congener, i.e., deserts and high mountains (Arnold, 1997;
Rieseberg, 1997). Their enhanced WUE presumably helps
these hybrid species to cope with the arid habitats and
establish initial populations. Our results further suggest
that the enhanced instantaneous water use efficiency of the
two hybrid genotypes is closely correlated with increases
in their leaf nitrogen contents per unit area (N
area
). This
is probably because the photosynthetic enzymes and
pigments represent a major investment in leaf nitrogen
(Field and Mooney, 1986). However, the nitrogen
concentrations per unit mass (N
mass
) did not exhibit such
a trend, since this parameter was higher in H. neurocarpa
than in H . rhanmoides ssp. sinensis and intermediate
in the two H. goniocarpa types. This may be due to the
differences in leaf thickness between the four genotypes.
While we here focused on differences in physiological
traits between H. goniocarpa and the parental species, it
should be noted that this species differs from the parental
species in the other traits.
For example, the germination
rate of this species is higher than that of the parental
species (Lian et al., 1998). In addition, we found that
seedlings of this species grow faster than those of both
parental species. The reproductive isolation of homoploid
hybrid species may arise through rapid chromosomal
repartitioning, ecological divergence and/or spatial
separation (Buerkle et al., 2000). Amongst these processes,
ecological divergence may be especially important, at least
according to simulations indicating that such speciation
is unlikely to occur in the absence of niche separation
(McCarthy et al., 1995). Hippophae goniocarpa occurs
sympatrically with the two parental species without spatial
separation, but the ecological divergence in this hybrid
species in flowering parameters (Lian et al., 1998) and
reproductive isolations may arise from a combination of
all these different performances, which may also together
provide inherent power to combine all individuals of two
genotypes as a distinct species unit.
Differences in physiological
performances
between the two maternal genotypes
Despite their concordant and positive transgression in
some physiological traits, our results suggest that there
are distinct differences in physiological
performances
between the two maternal genotypes of H. goniocarpa.
Apart from the total N concentration and transpiration
(E), all of the other traits showed distinct differences
between the two genotypes; A
max
, A
max
/E, CE, QE, NPQ,
LCP, long-term WUE (£_
13
C), N
area
, MSLA, LMA and C.
QE, CE, N
area
, LMA and long-term WUE (£_
13
C) were
higher in H . goniocarpa-N than in H . goniocarpa- R
while the contrary trends were found for A
max
, A
max
/E,
NPQ, LCP, MSLA and C. We initially expected these
differences to show correlations with the maternal species,
i.e. traits with high values in the maternal species to have
high values in the hybrid genotypes of H . goniocarpa
they respectively mothered. However, we did not detect
such overall correlations among all examined traits
(P > 0.05). For example, A
max
and A
max
/E were higher
in H . neurocarpa than in H. rhanmoides ssp. sinensis,
but lower in H. goniocarpa-N, mothered by the former
species than in H. goniocarpa-R, mothered by the latter
species. The differences in the other traits, i.e., QE, CE,
NPQ, long-term WUE (£_
13
C), N
area
, MSLA, LMA and C
concentrations in the two H. goniocarpa genotypes agree
well with the differences between their maternal species. If
the maternal species showed a higher value in one of these
traits, the mothered H. goniocarpa genotype accordingly
had a higher difference than the genotype mothered by
the other species. These differences suggest that maternal
origins have not had direct effects on the hybrid progeny.
Table 3. Positive (Pos) and interme dia te physiological m easurements of two hybrid genotypes (H. goniocarpo-N and H.
goniocarpo-R, mothered respectively by H. neurocarpa and H. rhamnoides) related to two parental species.
Traits
Hybrid genotype
H. goniocarpa-N
H. goniocarpa-R
A
max
(£gmol CO
2
m
-2
s
-1
)
E (mmol H
2
O m
-2
s
-1
)
A
max
/E
QE
CE
LCP
N
area
(g/m
2
)
LMA (g/m
2
)
MSLA (cm
2
)
£_
13
C
N%
C%
intermediate
neg. transgressive
pos. transgressive
neg. transgressive
pos. transgressive
neg. transgressive
pos. transgressive
pos. transgressive
intermediate
pos. transgressive
intermediate
neg. transgressive
pos. transgressive
neg. transgressive
pos. transgressive
neg. transgressive
rhanmoides-like
pos. transgressive
pos. transgressive
neurocarpa-like
intermediate
intermediate
intermediate
neg. transgressive
pg_0007
MA et al. ¡X Maternally-dependent physiological performances of
Hippophae goniocarpa
177
Instead, the physiological traits of these two genotypes
appear to have arisen from hybrid recombination and
ecological processes from those of both parental species.
The observed differences between the two maternal
genotypes of H. goniocarpa may reflect their differences
in ecological preference. For example, the higher A
max
in
H . goniocarpa-R implies that its growth may be faster
due to more rapid biomass accumulation (Aarssen and
Clauss, 1992; Arntz et al., 1998, 2000; Aarssen and
Keogh, 2002). In addition, the higher non-photochemical
quenching (NPQ) of chlorophyll fluorescence in this
genotype may facilitate its occupation of high altitude
habitats by allowing it to dissipate excess light in the form
of non-radiative energy to avoid or mitigate photodamage
to its leaves through the presence of high xanthophyll
contents (Xu et al., 1998; Zhao and Wang, 2002; Zhao et
al., 2007). The differences in both instantaneous (A
max
/E)
and long-term (£_
13
C) indices of water use efficiency
between the maternal genotypes may reflect differences
in water availability in their habitats, and thus their
habitat preferences. If so, the findings indicate that these
different maternal genotypes may occupy more distinctly
different habitats during their range expansion in the
future. Accordingly, available data regarding the molecular
phylogeography of other diploid hybrid species suggest
that different maternal genotypes usually inhabit different
regions (Brochman et al., 2000; Wang et al., 2001;
Schwarzbach and Rieseberg, 2002; Gross et al., 2003).
The differences in physiological performances between the
maternal genotypes found in the present study may partly
explain the general differences in distribution of different
maternal genotypes of natural hybrid species, in addition
to founder effects during their range expansion.
Acknowledgments. We are grateful for Dr Liu Jianquan
for his guidance and supervision of this research. He
also polished English of the final manuscript. Support
for this work was provided by the National Natural
Science Foundation of China (grant no. 30430560 and
30600041), FANEDD 200327 and a special grant from the
Ministry of Education of the People¡¦s Republic of China
(NCET-08-0257).
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MA et al. ¡X Maternally-dependent physiological performances of
Hippophae goniocarpa
179
>
pg_0010