| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
Plant Physiology 134:502-509 (2004) © 2004 American Society of Plant Biologists Is Each Light-Harvesting Complex Protein Important for Plant Fitness?1,[w]Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, S-901 87 Umeå, Sweden
Many of the photosynthetic genes are conserved among all higher plants, indicating that there is strong selective pressure to maintain the genes of each protein. However, mutants of these genes often lack visible growth phenotypes, suggesting that they are important only under certain conditions or have overlapping functions. To assess the importance of specific genes encoding the light-harvesting complex (LHC) proteins for the survival of the plant in the natural environment, we have combined two different scientific traditions by using an ecological fitness assay on a set of genetically modified Arabidopsis plants with differing LHC protein contents. The fitness of all of the LHC-deficient plants was reduced in some of the growth environments, supporting the hypothesis that each of the genes has been conserved because they provide ecological flexibility, which is of great adaptive value given the highly variable conditions encountered in nature.
Photosynthesis is one of Nature's most complex biochemical processes, and many hundred proteins are probably involved in it. Many of these proteins have been studied in great detail, and their functions are well known, whereas others have functions that remain obscure. The photosynthetic proteins generally show very high degrees of conservation. Although several differ between higher plants and cyanobacteria, the differences between green algae and higher plants are relatively small. Among seed plants (angiosperms and gymnosperms), the major photosynthetic proteins, like subunits of PSI and PSII, the cytochrome b6f complex, the ATP synthase, and the enzymes of the Calvin cycle seem to be present in all plant species and highly conserved between them.
Although these observations indicate that strong selection pressure must be present to maintain the genes encoding each protein, surprisingly large numbers of the genes have been knocked out using reverse genetic approaches without giving rise to obvious growth phenotypes (for review, see Scheller et al., 2001
To test the hypothesis that individual genes are important for the plants, we recently have developed an assay to measure the fitness of Arabidopsis plants under natural conditions by measuring seed production (Külheim et al., 2002
A Collection of LHC Protein-Deficient Arabidopsis Plants
To assess the specific function of each LHC protein, we have constructed and analyzed a collection of Arabidopsis plants that have suppressed levels of Lhca2, Lhca3, Lhca4, Lhcb1/Lhcb2, Lhcb4, or Lhcb5 and, thus, differ in LHC protein composition (Zhang et al., 1997
Southern-blot analysis showed that the knockout Lhca1 line contains one T-DNA insert only (data not shown). The Lhca1 knockout plants have the T-DNA insert in the promoter region (205 bp upstream of the translation start) of the Lhca1 gene. As a consequence, the plants contain a small amount (less than 10% of wild-type levels) of Lhca1 protein (Fig. 1). Levels of Lhca4 are also much lower than wild type in these plants, apparently because the stability of this protein is reduced in the absence of Lhca1, but the Lhca2 and Lhca3 levels are not affected. All Lhcb proteins are present in wild-type amounts in the Lhca1 knockouts (data not shown). In the Lhca4 transgenic plants (Zhang et al., 1997
We have summarized these data, together with previously published information, in Table I. It shows the LHC protein contents of the plants used in this experiment, grown under standard conditions in the growth chamber, on a reaction center basis. In the asLhcb2 plants, Lhcb1 is also lacking because of "cross-antisensing" (Andersson et al., 2003
To assess the importance of the LHC proteins in nature, we planted the collection of LHC protein-deficient plants in the field in a randomized block design together with their corresponding wild types. Because light is a critical parameter for photosynthesis, we decided to carry out the experiments in two different light regimes: in full sunlight and in the shade of trees. The site in full sunlight was homogenous in all respects, including irradiation. The irradiance pattern on a typical day can be seen in the supplemental material. There were, not surprisingly, large variations in irradiance both between days and during the day (see also Külheim et al., 2002 The unavoidable differences in planting dates between the subexperiments resulted in some unexpected consequences. Most notably, the asLhca4 plants and the corresponding wild type (C24) performed very poorly at the Sun site. Because these were the last to be planted out, they were the least capable of coping with the drought, which intensified during the course of the experiment. Also, when larvae of diamond-backed moths (Plutella xylostella) appeared, these plants were smaller than those of the other genotypes, so they were much more heavily affected, and mortality was pronounced. The number of surviving plants was too small to allow a meaningful analysis, so these plants were not further considered in the fitness experiment. Therefore, data for the asLhca4 plants are only available for the shade experiment for the year 2002. In Figure 2 data from a pre-experiment, performed in 2001, are shown instead. The 2001 site was intermediate between the 2002 sun and shade sites in terms of light quantity and variation.
Growth (in terms of germination rate and timing, rosette diameter, time of bolting, and inflorescence height) was followed for all plants throughout the experiment. Most genotypes showed no differences in growth compared with the corresponding wild type, but the asLhca4 plants grew more slowly and flowered significantly later than the wild-type plants (data not shown).
The transgenic plants were grown in the field until they had finished producing flowers. At this stage, the leaves were in a late stage of senescence, and the plants appeared to be almost dead. Seed production for each plant was calculated by multiplying the average number of seeds from three mature siliques by the total number of siliques (Külheim et al., 2002 At the Sun site, all Lhca lines produced fewer seeds than wild-type plants (Fig. 2A), although the difference was statistically significant only in the cases of Lhca2 and Lhca4. At the shade site, the koLhca1 plants produced the same number of seeds as the wild type, whereas Lhca2 produced fewer seeds and Lhca3 and Lhca4 significantly fewer seeds. The reduced seed production per plant was in most cases because of a decrease in the number of siliques per plant, but in a few cases, it was because of a decrease in seeds per silique or both of these factors (Fig. 2, C and E). The fitness reduction of the Lhcb lines at the Sun site was pronounced (Fig. 2B). All four lines produced significantly fewer seeds than wild-type plants. The effect in shaded conditions was less marked. asLhcb5 plants did not show any reduction in fitness, and the reduction for Lhcb2 was not statistically significant. The major effect found in the latter case was in the number of siliques per plant, but the number of seeds per siliques was significantly lower in the asLhcb6 line (Fig. 2, D and F). No significant difference in seed weight was observed for any of the lines (data not shown).
The fitness reduction was most pronounced for asLhca4 plants, and the growth of these plants was also severely impaired in terms of both inflorescence height and leaf rosette diameter, which in both cases reached only about 30% of wild-type levels in the shade (data not shown). Therefore, removal of Lhca4 by antisense inhibition seemed to affect Arabidopsis much more than removal of other Lhc proteins. In a pre-experiment to this study, performed in 2001, fitness was even more severely reduced, and the seed production of the Lhca4 antisense plants amounted to only 9% of the wild-type production (Fig. 2A). Thus, asLhca4 plants clearly performed much less well than wild-type plants.
Because growth was also heavily impaired in the asLhca4 plants, in contrast to the other lines where no apparent growth difference was seen, comparison of seed production between wild-type and asLhca4 plants is not as straightforward as with the other lines. In addition, flowering is somewhat delayed in this line, according to both a previous report (Zhang et al., 1997
In the field, plants are subjected to a wide range of stresses. Although stress can be manifested in many different ways, one useful parameter to monitor when stress to the photosynthetic apparatus occurs is the extent to which the plant is affected by photo-inhibition of photosynthesis. A convenient way to measure this, which can also be used in the field, is to record the chlorophyll fluorescence parameter (Fv/Fm), which decreases in all kinds of stress that result in increased excitation pressure of photosystem II. We have shown recently that plants that lack PsbS and, thus, feedback de-excitation, show reduced fitness in the field, and also increased levels of photo-inhibition (Külheim et al., 2002 As expected, the level of photo-inhibition of wild-type plants varied with the weather (higher irradiance leads to increased photo-inhibition) and increased at the end of the experiment, when the leaves showed quite severe symptoms of senescence. The pattern resembled trends we have observed previously in Arabidopsis plants grown in the field and is probably typical of annual plants with accelerated life cycles, such as Arabidopsis. We recorded photo-inhibition in all genotypes at both the sun and the shade sites. Typical results are shown in Figure 4, where Fv/Fm levels found are compared for the Lhcb2 antisense plants and wild-type plants. As can be seen, there was no significant difference in the amount of photo-inhibition between the two genotypes, so the absence of Lhcb1 and Lhcb2 does not seem to increase the amount of excitation pressure on the photosynthetic apparatus. Corresponding graphs for the other genotypes can be found in the supplemental material. These graphs show that we did not detect any significant difference in photo-inhibition in any of the genotypes, including the Lhca4 antisense plants (despite their strong growth phenotype in the field), so none of the genotypes were adversely affected by higher levels of photo-inhibition.
Since the publication of Darwin's theory on the survival of the fittest and Mendel's discovery of genetics in the late 19th century, scientists have been aware that the interaction between genotype and environment is a key determinant of the fitness of an individual. Nevertheless, there have been very few studies to date in which the contribution of a single, known gene product to plants' fitness in the natural environment has been quantified, partly for methodological reasons. Although huge numbers of plant mutants are available, there are far fewer cases where the mutation has been shown to result in the loss of a single defined gene product. More importantly, however, several different scientific traditions have to be combined. Molecular biologists grow mutants with known lesions in controlled environments without considering the fitness parameter, whereas ecologists generally grow poorly characterized plants in the natural environment and measure their fitness. To investigate the importance for plant fitness of single photosynthetic genes, we have developed an assay using Arabidopsis as a model plant (Külheim et al., 2002  ). For an annual plant like Arabidopsis, which flowers early in the season and produces seeds that germinate in the same year or the following spring, the ability to set seeds determines the survival of the species; therefore, relative seed production provides an accurate measure of relative fitness, provided that germination frequency is constant. Very recently, the same approach was used to study fitness effects of R-mediated resistance (Tian et al., 2003).
We already have reported a study of mutants lacking feedback de-excitation (Külheim et al., 2002
The general issue addressed in this study is the importance of each single protein in the photosynthetic apparatus for the plants. Although many proteins are clearly essential for photosynthesis, plants lacking any one of surprisingly large numbers of the proteins in the photosynthetic apparatus have shown no apparent growth aberrations. The LHC proteins may be particularly interesting in this respect because they constitute a family of proteins that share the general function of maximizing the efficiency of photosynthetic light harvesting, but none of them are essential for photosynthesis. This raises intriguing questions because if they do not each have a specific function, their evolutionary conservation is contrary to theoretical expectations. In a number of investigations, plants lacking specific photosynthetic proteins have grown normally under stress-free conditions, and they then have been exposed to abiotic stress (often suboptimal light or temperature) under controlled conditions and differences have sometimes, but not always, appeared (e.g. Niyogi et al., 1998 There are several potential problems with such a study. The plant material should be genetically homogenous. The antisense effect has to be stable under field conditions. It must be shown that seed production is an adequate measure of fitness in the test species. The genotype differences need to be large enough to be detectable despite the huge variations in growth (and, thus, seed production) in the field. The possibility that the transformation event per se may reduce fitness needs also to be considered, i.e. could the presence of the rest of the T-DNA be harmful for the plant under natural conditions? Also, the significant amount of manpower necessary to conduct the field experiments made it impossible to analyze more than one transgenic line lacking each protein. We believe that all of these potential problems have been addressed in this study, enabling us to draw rigorous conclusions from the results. First, inhomogeneity of genetic material is in normal experiments minimized by germinating seeds on selective plates. Although this was not possible here, errors introduced in this way could only result in underestimation of the reduction in fitness for a transgenic line since some of the "transgenic" plants would be wild type. Second, loss of the antisense effect in the field in some plant individuals will also result in an underestimation of fitness. Third, we believe that Arabidopsis seed production is a reasonably accurate measure of fitness. Several problems are associated with measuring the germination frequency of plants grown in the field. To maximize germination frequency, Arabidopsis seeds should be left on the plants until the siliques open and the seeds are dispersed. Here, we could not do this because all seeds were harvested at the same time; hence, germination tests would not have been reliable. However, plants with reduced seed production are also likely to produce a smaller proportion of viable seeds, which will probably result in an underestimation of the true fitness reduction. Fourth, a strict experimental approach was adopted, in which the genotypes were grown in a fully randomized block design because even plants of the same genotype growing close to each other can often display very different traits because of stochastic events, e.g. attacks by herbivores. We do not believe that the rest of the T-DNA (e.g. the resistance marker) has any negative effect on the fitness. We performed an identical analysis with similar transgenic lines lacking proteins with less obvious functions and lines overexpressing different proteins. None of these plants exhibited any reduction in fitness, suggesting that the rest of the T-DNA is unlikely to have an effect on fitness. In addition, the data are consistent with theoretical expectations: Plants lacking a large portion of the antenna (e.g. asLhca4) show a more pronounced reduction in fitness than those with deficiencies where the overall effects on protein content were more minor, e.g. Lhca1. Finally, in all cases but the koLhca1 line, where only one line is available, we have in the original publications analyzed several lines of each construct in the lab, and we always observed consistent phenotypes. This is also true for asLhcb6 (data not shown). The data for Lhca1, therefore, are weaker, but because the Lhca1 plants were the ones where we saw the smallest effect, we think that this will not be important for the conclusions of the paper. Therefore, we believe that the effects we observed are, genuinely, consequences of the loss of individual LHC proteins. We cannot exclude the possibility that the effect is indirect (i.e. because of decreased integrity if the whole antenna system in the absence of the target protein) but that does not change the main conclusion that each protein has a unique function.
The LHC contents in the field may differ because the total and relative levels of LHC protein vary with changes in conditions (Bailey et al., 2001
Plants in the field are subjected to a wide range of stresses, such as differences in light intensity and quality, drought, and grazing. As expected, the experimental plants showed a variety of stress responses, such as early flowering, small, thick leaves, pronounced anthocyanin production, and leaf necrosis. However, none of the transgenic lines exhibited more photo-inhibition of photosynthesis than the corresponding wild type, unlike mutants lacking PsbS or violaxanthin de-epoxidase, which are proteins with a photoprotective function (Külheim et al., 2002 Under the uncontrolled conditions used here, the huge variation in performance of individuals of the same genotype necessitates the use of large numbers of plants to detect significant differences between the genotypes. Scaling up creates logistic problems, but for seven of the eight genotypes, we found a statistically significant decrease in fitness under some conditions. Not surprisingly, the effect differed greatly between the subexperiments. In a pre-experiment, performed in 2001 (see supplemental material), the Lhca4, Lhcb2, Lhcb4, Lhcb5, and Lhcb6 lines all showed a greater decrease in fitness, especially in the shade, probably because the weather conditions were less favorable and/or grazing was different. By far, the largest effect in 2002 was found in the asLhca4 line, which produced only 32.5% of the wild-type amount of seeds (shade). In 2001, fitness reduction was even more pronounced: asLhca4 plants produced on average only 9% as many seeds as the wild type. These plants also showed growth retardation in the climate chamber, unlike the other genotypes. Presumably, the loss of most of the light-harvesting antenna of PSI caused an imbalance in electron transport, which impaired the performance of the plants, and this will be the subject of a coming study. It may appear surprising that we were able to detect a clear effect on fitness in plants that did not differ in growth rate. We believe that the higher sensitivity of the fitness assay is because of the fact that the production of reproductive structures puts high demands on the photosynthetic apparatus. Before flower formation, photosynthetic efficiency may be slightly affected without affecting growth rates, but when flowers and later seeds are formed, very strong sinks are created. Under such circumstances, even minute differences in light harvesting could reduce maximum photosynthetic capacity, leading to significantly reduced flower formation and, thus, seed set. It may be surprising, given that the missing proteins are antenna proteins, that the reductions in fitness were higher under high-light conditions in some cases, but we believe that this finding should be treated with caution. In the pre-experiment in 2001, fitness reduction was much more pronounced under shaded conditions. However, the site used that year was different from those used in 2002, and the shading was much more irregular, resulting in larger variations in irradiance. If data from both years are taken into consideration, it may be concluded that the LHC proteins, like PsbS, have a major role in adjusting the light-harvesting antenna in response to variations in light conditions, but more detailed studies are required to determine the types of light conditions that are particularly harmful to the different genotypes. At present, we can only conclude that most, and probably all, of the studied proteins have a significant effect on plant performance under natural conditions, supporting the view that each LHC protein is important for plant fitness.
Plant Material
Arabidopsis ecotypes Columbia or C24 were used as genetic background for the construction of LHC protein-deficient antisense plants as previously described. The antisense (as) Lhca4 (line 22) is described by Zhang et al. (1997
For experiments under controlled conditions, Arabidopsis plants were grown under fluorescent lamps in a growth cabinet with a day/night temperature regime of 23°C/18°C, a photoperiod of 8 h with a light intensity of 150 µmol m-2 s-1 quanta, and 75% humidity. For the fitness experiment, plastic trays with drainage holes were filled with soil and pots without bottoms (with three seeds from either wild-type or antisense plants) were randomly positioned in the tray to avoid position-dependent differences in growth affecting the results. The seeds were stratified for 4 d and then placed in the field. When seedlings appeared, one per pot was chosen for the experiment, and the others were removed. The field experiments were performed in the experimental garden of Umeå University (Sweden; 63° 50'N, 20° 20'E). Because these plants are genetically modified organisms, permission to grow the transgenic lines in the field was applied for and given by the Swedish Board of Agriculture (Jordbruksverket). Details about the permit and measures taken to prevent contamination of the environment by transgenic seeds or pollen are available on request. Three sites were cleared of vegetation: one in full sunlight (hereafter named sun) and two in the shade of trees growing at the site (Shades A and B). The distance between the shade sites was less than 5 m, and they were about 50 m from the sun site. Ten centimeters of soil were replaced with new soil, and the plastic trays were placed out in the field, giving soil-to-soil contact. For practical reasons, not all genotypes could be planted at the same time on all sites. The Lhcb2, Lhcb4, Lhcb5, and Lhcb6 antisense plants and Columbia wild type were planted out on sun and Shade B on June 24. A second set of genotypes (Lhca1, Lhca2, and Lhca3 antisense plants plus Columbia wild type) was transferred to the sun and Shade A sites on July 12. Finally, Lhca4 and C24 wild type were planted out at the sun and Shade B sites on July 17. The irradiation of the three sites was recorded for typical days using a quantum sensor (Skye SKP 215, Skye Instrument Ltd., Llandrindod Wells, UK), and data were recorded and stored with a data logger (CR 10, Campbell Scientific Ltd., Logan, UT), other weather parameters were logged about 200 m from the sites, and these data are available at http://www.tfe.umu.se/weather/arkiv.asp. In general, the summer in the area was unusually dry and warm. The intention was to expose the plants in the field experiment to conditions that were as natural as possible, without watering, fertilization, or protection against pests. However, to avoid all the small seedlings dying through drought, some water had to be added early in the experiments, and after a heavy attack of diamond-backed moths (Plutella xylostella), insecticide (Pyrex N, Wikholm & Co., Stockholm) was applied once. When the plants started to flower, the site was covered with a net to prevent insects reaching the plants and, thus, reduce the probability of spreading transgenic pollen. The experiment was terminated between mid-August and early September, depending on the genotype and experimental site. When harvested, most plants appeared to be dead, and no more flowers were produced.
Leaves of Arabidopsis plants (6-8 weeks old) grown under controlled conditions were taken for thylakoid protein preparation 3 h into the growth period according to Zhang et al. (1997
A block design was used in which all genotypes in a subexperiment were fully randomized in a tray containing 30 plants. For example, at "sun", six seedlings each of the Lhcb2, Lhcb4, Lhcb5, Lhcb6, and Columbia genotypes were placed in each tray. Three to nine trays, all individually randomized, were used in each subexperiment in each area, the total number of plants of each genotype was at least 40 per area, and the total number of plants in the whole experiment was 1,050.
For each experimental plant, the total number of siliques was counted, and seeds were counted from three randomly chosen mature siliques. The total number of seeds was then calculated for each plant by multiplying the average number of seeds per silique by the number of siliques. The seeds from the three siliques were pooled and weighed (to the nearest 0.001 mg), giving an estimate of total seed weight.
A plant stress meter (Techtum Lab, Umeå, Sweden) was used to measure the fluorescence parameter Fv/Fm in intact plants in the field according to Öquist and Wass (1988
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third party owners of all or parts of the material. Obtaining any permission will be the responsibility of the requestor.
Lars Ericsson is thanked for providing growth space for the experiments, Martin Frenkel for plant care, Kristin Palmqvist for help with recording light curves at the experimental sites, and Jon Moen for valuable help with the statistical analysis. Received September 15, 2003; returned for revision October 16, 2003; accepted October 16, 2003.
1 This work was supported by the Swedish Research Council, by the Swedish Research Council for the Environment, by Agricultural Sciences and Spatial Planning, and by the European Community's Human Potential Programme (contract no. HPRN-CT-2002-00248 [PSICO]). 
[w] The online version of this article contains Web-only data.
2 These authors contributed equally to the paper. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.033324. * Corresponding author; e-mail ulrika.ganeteg{at}plantphys.umu.se; fax 46-90-786-66-76.
Andersson J, Walters RG, Horton P, Jansson S (2001) Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13: 1193-1204 Andersson J, Wentworth M, Walters RG, Howard C, Ruban AV, Horton P, Jansson S (2003) Absence of Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II-effects on photosynthesis grana stacking, and fitness. Plant J 35: 350-361[CrossRef][Web of Science][Medline] Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213: 794-801[CrossRef][Web of Science][Medline]
Elrad D, Niyogi KK, Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14: 1801-1816
Ganeteg U, Strand Å, Gustafsson P, Jansson S (2001) The properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition. Plant Physiol 127: 150-158 Haldrup A, Naver H, Scheller HV (1999) The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem I. Plant J 17: 689-698[CrossRef][Web of Science][Medline]
Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants form photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96: 8762-8767 Jansson S (1994) The light-harvesting chlorophyll a/b binding-proteins. Biochim Biophys Acta 1184: 1-19[Medline]
Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297: 91-93 Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395[CrossRef][Medline]
Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134 Öquist G, Wass R (1988) A portable, microprocessor operated instrument for measuring chlorophyll fluorescence kinetics in stress physiology. Physiol Plant 73: 211-217 Ruban AV, Wentworth M, Yakushevska AE, Andersson J, Lee PJ, Keegstra W, Dekker JP, Boekema EJ, Jansson S, Horton P (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421: 648-651[CrossRef][Medline] Scheller HV, Jensen PE, Haldrup A, Lunde C, Knoetzel J (2001) Role of subunits in eukaryotic Photosystem I. Biochim Biophys Acta 1507: 41-60[Medline] Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74-77[CrossRef][Medline] Zhang H, Goodman HM, Jansson S (1997) Antisense inhibition of the photosystem I antenna protein Lhca4 in Arabidopsis thaliana. Plant Physiol 115: 1525-1531[Abstract] This article has been cited by other articles:
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | PLANT PHYSIOLOGY® | THE PLANT CELL | |
|---|---|---|---|
TOP
ABSTRACT
RESULTS
30). A and B, Total seed count per plant. C and D, Number of siliques per plant. E and F, Number of seeds per silique. The statistical significance of deviations from wild type is showed by asterisks: (*), P < 0.1; *, P < 0.05; **, P < 0.01; ***, P < 0.001; 
, experiment from 2001.
