Therefore, factors other than the duration of the SFP are responsible for the documented variation in composition with nodal position. Our results raise the question of whether soy food products made from seed from different portions of the canopy would vary in terms of their mineral concentrations. Three of the most common and simplest products to make from soybean seeds are flour, milk and okara the particulate material remaining after preparation of milk.
Because Fe is one of the most critical minerals to human health and anemia is a global epidemic, we focused our initial analysis on the Fe content of these soy food products. We prepared flour from seven lines, and milk and okara from four lines and Fig. With all three products, the concentration of Fe was highest in products made from seeds produced at the bottom of the canopy and decreased progressively with canopy position of the seeds used. Thus, as would be expected the concentration of seed Fe affects the concentration of Fe in the flour, milk or okara produced from those seeds.
Although many questions remain, the public health implications of our findings are apparent. Given that mineral content of seeds, especially Fe, is important our results uncover another source of variation that can be directly exploited. The canopy effect on seed mineral concentration prompted us to look at the distribution of minerals in the shoots of vegetative plants. Consequently, we examined the leaf ionome from four genotypes as a function of canopy position. Na and Ni were present at low absolute concentrations and fluctuated but not in a progressive pattern as for the other minerals.
The basis for differential accumulation of foliar minerals at different positions within the canopy is not clear and will be important to address in future studies. One possible explanation is that the greater phloem mobility of P and K facilitates their enhanced remobilization to upper nodes whereas other less mobile elements e. This would not readily explain the observed profiles for Cu, Zn and Mo, however, highlighting the complexities involved in metal homeostasis and the significant variation with canopy position.
Another working hypothesis could be that K, P, Cu, Zn and Mo are mineral markers of metabolic activity and accumulate in leaves at the top of the canopy that have highest rates of photosynthesis. Opposite patterns were observed for other minerals Ca, Mn, and Cu suggesting that remobilization is either mineral specific or not quantitatively important in delivery of minerals to developing seeds. A final point to note is that the potential exists for some soil particles to adhere to vegetative plant parts, especially lower in the canopy, while seeds are protected from soil contamination by the pods.
Since some minerals exhibited opposite patterns, it seems that soil adhesion could not be completely responsible for the patterns observed. Developing seeds were analyzed to determine whether canopy position affected seed metabolism sufficiently to explain the observed differences in protein and oil concentrations at maturity. All seeds were at the stage of development where cell expansion and accumulation of storage compounds protein and oil were the dominant metabolic processes Collakova et al. Untargeted metabolite profiling was conducted for analysis of polar compounds, free amino acids, free fatty acids, and total fatty acids File S7.
In general, most metabolites did not show diurnal changes in concentration, but there were differences in concentrations as a function of seed size and node position. The metabolite plots in Fig. The concentration of sucrose Fig.
The decrease in sucrose concentration comparing top seed on day 1 and day 7 likely reflects in part the dilution effect caused by storage product accumulation as the seeds increased in size by roughly 2-fold. In contrast, the concentration of citrate in developing seeds was roughly equal among the three samples Fig. These results suggest that seeds actually accumulate sucrose and to a larger extent citrate as they increase in dry matter during seed fill thereby negating the dilution effect caused by seed growth.
This also indicates that developing seeds have ample sugars and organic acids irrespective of size and node position and time of day. In marked contrast to sucrose and citrate were the dramatic differences observed in free asparagine Asn concentration Fig. The roughly 2-fold decrease in Asn concentration in seeds at the top of the canopy from day 1 to day 7 likely reflects the dilution effect of growth. The pattern for Asn concentration is potentially of interest because free Asn concentration during seed development correlates with protein concentration at maturity Herman, ; Hernandez-Sebastia et al.
The results obtained in the present study suggest that greater supply of Asn to developing seeds at the top of the canopy may contribute to the observed greater accumulation of storage protein. Importantly, Asn was also one of the important metabolites that distinguished the three sets of seeds collected based on a global metabolite analysis File S8. Mean values for Asn, and other protein amino acids are shown in Fig. The concentrations of the free amino acids was highest in the small seed top seed, day 1. Concentrations of Ala, Asn, Gly, and Thr were substantially higher in top seed at day 7 relative to bottom seed at day 1 when seed sizes were similar.
Of those amino acids, Asn was present at the highest absolute concentrations and may contribute to the storage protein biosynthesis either by acting as a signal metabolite or providing substrate for protein biosynthesis. The present study yields two major conclusions. First, the position along the main stem at which soybean seeds develop has a profound impact on seed composition, affecting the concentrations of protein, oil and certain minerals at maturity. Second, the canopy position effects on seed mineral concentrations in particular Fe are sufficiently large that there may be direct implications for human nutrition in countries where plants are the main source of protein and soybeans are used for human food.
These conclusions are discussed in more detail below. Results of the present study demonstrate that for 10 lines grown over a period of 3 years there were remarkably consistent gradients in protein and oil concentrations in mature seeds as a function of nodal position Figs. However, oil accumulation tends to plateau before protein accumulation and therefore, percent oil will often decrease with increasing duration of the SFP rather than increase.
In the present study, the protein and oil concentration gradients from bottom to top of the canopy were not correlated with the difference in SFP between the two positions Fig. Micro-environment appears to be one factor controlling protein and oil concentration gradients in the canopy because removal of neighboring plants at flowering increased protein concentration at all positions and decreased the difference between top and bottom nodes Fig.
While it is not clear which micro-environmental factor s might actually be involved, we suggest that increased light energy reaching lower leaves may be a contributing factor. Metabolomic analysis of developing seeds that identified free Asn as one of the primary metabolites distinguishing seeds at the bottom and top of the canopy supports this conclusion. Asparagine is the major free amino acid in developing soybean seeds and differences in Asn concentration during development are positively correlated with protein concentration at seed maturity Hernandez-Sebastia et al.
Furthermore, over-expression of asparaginase in soybean, driven by an embryo-specific promoter, resulted in a reduction in free Asn concentration during development and reduced protein concentration in mature seed, measured by nitrogen analysis Pandurangan et al. Collectively, these results suggest that free Asn is a sensor or regulator of processes that determine protein accumulation in soybean seeds Herman, Our results are consistent with this hypothesis and suggest that differences in free Asn concentration may explain the position effects on seed protein and oil concentration.
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We speculate that decreased light at lower positions in the closed canopy i. These differences could reflect alternate routes from the apoplast to the symplast or differences in mobility in the phloem White, Interestingly, minerals that tended to have highest concentrations in seeds at the bottom of the canopy e. These results suggest that remobilization from leaves may be playing some role at least in the positional effects on the mature seed ionome.
Sources of variability in canopy reflectance and the convergent properties of plants
Another factor that may impact the distribution of minerals in seeds along the mainstem is precipitation. This speculation is based on the increased concentrations of Ca, Mn, and Sr found in seeds at the top of the canopy in , which had above normal precipitation. It is possible that increased precipitation resulted in greater xylem transport of certain minerals including Ca, Mn, and Sr to developing seeds at the top of the canopy, or alternatively, that weather conditions in allowed greater remobilization of selected minerals from leaves via the xylem.
It is recognized that while Ca and Mn are generally considered to have very low phloem mobility and are therefore not remobilized from senescing leaves, there is variation among species in the extent of remobilization Maillard et al. Conceivably, remobilization may also be triggered from leaves of all species under certain conditions. While multiple seed constituents exhibited canopy concentration gradients, it seems unlikely that they are all caused by the same factors. Changing the microenvironment by thinning plants to allow increased light penetration into the canopy altered the protein and oil gradients but did not affect observed gradients for most of the minerals Fig.
Furthermore, while the slope of many gradients changes across lines, treatment and year, the way that they change is not well correlated between the different constituents, as illustrated in the plot normalized correlation matrix Fig. However, numerous correlations were apparent when mean plot values were compared Fig. Several minerals e. Thus, some coordination between seed storage product accumulation and mineral uptake into seeds is evident. It should be noted that altering the microenvironment by thinning plants did affect the observed gradients in seed concentrations of Ca, Mn, and Sr, which were also the minerals altered in distribution in the year of this study with above normal precipitation.
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These results highlight the differences among minerals in terms of factors controlling their distribution among seed produced at different node positions. Clear, continued studies in the future will be required to sort out the different mechanisms involved. Soybeans are valued for their protein and oil content, but when used for human nutrition the content of minerals such as iron and zinc is also critically important.
On a global scale, human iron deficiency is one of the most prevalent nutritional disorders McLean et al. As discussed above, nodal position affected the concentration of several minerals such as Mg, Fe, and Cu that were present at higher concentrations in seeds produced at the bottom of the canopy. Soy flour preserved more Fe than did milk; perhaps mineral retention improvement through product preparation is possible.
An immediate application of our results with respect to human nutrition would be to use seeds from the top and bottom halves of the canopy for different purposes, with seeds produced in the lower half reserved for production of iron-rich soy foods for human consumption. Thus, knowledge of these canopy position effects provides an unexpected approach to link agronomic practices to improve human nutrition and health. Overall, our results raise a number of questions and directions for future research. For example, it would be interesting to explore whether there are positional effects on soybean seed functional traits such as seed vigor or seedling stress tolerance.
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Because environment during reproductive development of plants is now recognized to broadly impact seed properties, such as growth performance and stress tolerance of the progeny Biodner et al. Our results also raise the question of whether similar effects occur in other species including non-domesticated plants where there might be some ecological significance.
Another area that will be interesting to explore is the impact of elevated CO 2 on the canopy positional effects described in the present study. It was recently reported Loladze, ; Myers et al.
It is relevant to note that variation in seed Fe concentration with node position established in the present study is substantially larger 4-fold greater compared to the impact of climate change on mean seed Fe concentration. Therefore, our results are likely to be meaningful from a quantitative standpoint and have important implications for examining the impact of climate change on the seed ionome.
Identifying the molecular mechanisms underlying canopy gradients in composition may provide new approaches to controlling soybean seed quality for various uses, including food for human consumption under conditions of global climate change. Common use cases Typos, corrections needed, missing information, abuse, etc. Our promise PeerJ promises to address all issues as quickly and professionally as possible.
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View article. Rishi R. Masalia RishiMasalia days ago. Jennifer Mach JenniferMach2 days ago. Chris Pires JChrisPires days ago. Ivan BaxterTwi days ago. Materials and Methods Plant growth and sampling Soybean lines were grown at the University of Illinois South Farm, Urbana, IL, in a randomized complete block design with three replicates each year. Ionomic analysis Seed analysis was conducted as described in Ziegler et al. Data analysis Protein, oil, and elemental data were analyzed using R and the packages dplyr, ggplot2, grid, reshape2, qtlcharts and gplots.
Download full-size image. DOI: Interactive Correlation plots of all plot normalized data DOI: Interactive Correlation plots of plot mean data DOI: Interactive Correlation plots of all data, not normalized DOI: Composiition of food products for all elements DOI: At similar tree density per hectare, the different growth conditions along the altitudinal gradient resulted in a more open canopy at high altitudes.
This was reflected in lower LAI values and subsequently increased the penetration of light into the canopy Table 1. Similarly, Lowman had reported that warm temperate forests have higher LAI when compared with cold temperate forests, and that this results in lower transmission of light through the canopy 5.
Canopy structure thus has a key effect on the penetration of solar beams into lower canopy depths. The crowns of all trees were thus considerably differentiated into a sunlit and a shaded part at all altitudes investigated. Our results show a great capacity for F. We found evidence supporting the hypothesis that the climatic conditions along the altitudinal gradient modulate the structure of forest canopies and thereby alter the local light environment. In particular, the limiting role of low light intensities is pronounced under favourable climate conditions of low altitudes.
A less limiting role of light was meanwhile observed under climate-limiting conditions of high altitudes, where the canopies achieve lower LAI values Table 1. As discussed below, such asymmetrical acclimation resulted in a convergence of morphological, biochemical and physiological traits of upper and lower canopy leaves with increasing altitude. It has been reported that LMA and N area increase with altitude in some functional groups like forbs and angiosperm trees but do not vary in conifers Williams et al.
Our results for F. To the best of our knowledge, such an asymmetrical response has not previously been reported. Leaf mass per area is significantly modulated by, among other factors, light intensity, temperature and nutrient availability Poorter et al. Higher transmittance of light into lower canopy depths at high altitudes Table 1 is likely the most important reason for increased LMA of lower canopy leaves.
In addition, however, developmental constraints on high-elevation plants may decouple leaf N content from soil N content due to restricted root activity at low temperatures Pregitzer et al. These hypotheses are supported, respectively, by the relatively low differences in N area values of leaves Figure 3 , which are in contrast to the large differences in total N content in soil across the altitudinal gradient Table 2 , or by higher N area values in lower canopy F. Finally, the decrease in temperature with higher altitudes may additionally contribute to an increase in LMA of lower canopy leaves.
For example, Atkin et al. This was associated with increased photosynthetic capacity, thus demonstrating cold acclimation of lowland species. We found a decrease in total chlorophyll content in upper canopy leaves at the highest altitude studied, which is in accordance with the literature Roblek et al. The total chlorophyll content in lower canopy leaves presented the opposite trend, however, as it increased with altitude.
Accordingly, upper and lower canopy leaves at the highest altitude had approximately the same amount of chlorophylls Figure Evans and Poorter had found that changes in LMA and N partitioning between proteins and photosynthetic pigments within leaves are closely coupled in the process of light acclimation. Plants grown in low-light conditions partitioned a larger fraction of leaf N into light-harvesting proteins and proteins associated with effective photochemical reactions on thylakoid membrane Boardman , Seemann et al.
In addition, we observed a significant increase in flavonol content in lower canopy leaves along the altitudinal gradient, whereas no differences between altitudes were observed in upper canopy leaves Figure We found strong relationships between C area Figure 3 c and d and accumulation of epidermal flavonols, which is in accordance with the previous finding that the biosynthesis of flavonoids, particularly phenylpropanoid-derived compounds, is closely related to carbon—nutrient balance Koricheva et al.
The synthesis of C-based secondary metabolites is further determined by specific demands e.
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The synthesis of flavonoids, tannins and hydroxycinnamate esters, among other metabolites, may thus represent an alternative pathway for the dissipation of excessive radiation energy and consequently may contribute to enhanced antioxidant capacity of the cell Grace and Logan , particularly under the stress conditions of high elevations.
Rubisco content per unit leaf area in upper and lower canopy leaves tended to converge at higher altitudes Figure 7 , particularly due to reduced Rubisco content in upper canopy leaves. This is consistent with a gradually decreased allocation of N to Rubisco in upper canopy leaves with increasing altitude Figure 8. It is consistent, too, with previous findings that cold acclimation of plants, including induction of antifreeze proteins and changes in membrane composition Janda et al.
Although the paradigm of N-based photosynthetic machinery assumes that N-containing enzymes are fully active, several studies have shown that Rubisco may not be fully active in naturally growing leaves Eichelmann et al. The relatively low A max at high Rubisco contents observed in trees at low altitudes indicates Rubisco to be in enzymatically inactive forms. This may imply that inactive Rubisco serves as N storage, especially in upper canopy leaves of trees growing at low altitudes Figure 9. Similarly, Sakata et al. Schmidt H. Hara along an altitudinal gradient as well as during the vegetation growing season.
The activity of photosynthetic enzymes—in contrast to light absorption—is reduced at low temperatures and thus leads to an increased risk of photo-oxidative damage Tsonev and Hikosaka The aforementioned changes in morphological and biochemical traits of leaves consequently result in a convergence of physiological functions of upper and lower canopy leaves at higher altitudes, and in particular of assimilation capacity A max ; Figure 4 a and b and light-use efficiency as measured by the proxy PRI Figure 6.
The rate of CO 2 uptake, however, was significantly controlled by stomatal conductance Figure 5. In July, the hottest and driest period, the highest stomatal conductance was found for altitude M, likely the site with the greatest local water availability. As PRI has been associated with photosynthetic light-use efficiency Gamon et al. This phenomenon has been observed previously for Quercus ilex L.
Such acclimation to low-light intensities is regarded as a typical response of shade-intolerant species Kubiske and Pregitzer Nevertheless, restricted growth conditions associated with high altitudes have a potential to stimulate biochemical acclimation represented for example by changes in N area , chlorophyll and Rubisco contents in lower canopy leaves of F. Generally, with increasing altitude lower canopy leaves tended to acquire the same traits as upper canopy leaves.
Nevertheless, there were strong vertical gradients in light intensity across a canopy at all altitudes investigated. Under similar stand density, restrictive growth conditions result in a more open canopy and higher penetration of light into lower canopy with increasing altitude. The beech forest responded mainly by changing the traits of lower canopy leaves along the elevation gradient and thus showed a great capacity for the tree to adjust its entire canopy to cope with changing conditions.
Such plasticity in the acclimation of leaves has the potential to cause a substantial change in the photosynthesis of forest canopies and in their contribution to the overall C balance of vegetation. Supplementary data for this article are available at Tree Physiology Online. Participation of PhD students P. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign In. Advanced Search. Article Navigation. Close mobile search navigation Article Navigation.
Volume This article was originally published in. Article Contents. Materials and methods. Supplementary data. Conflict of interest. Oxford Academic. Google Scholar. Karel Klem. Petr Holub. Albert Rivas-Ubach. Jordi Sardans. Michal V. Otmar Urban. Article history. Cite Citation. Permissions Icon Permissions. Abstract The present work has explored for the first time acclimation of upper versus lower canopy leaves along an altitudinal gradient. Figure 1. View large Download slide. Table 1. View Large.
Table 2. Figure 2. Figure 3. Figure 4. Figure 5. Figure 6. Figure 7. Figure 8. Figure 9. Figure High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric. Search ADS. De Frenne. Latitudinal gradients as natural laboratories to infer species' responses to temperature. Adjustment of leaf photosynthesis to shade in a natural canopy: reallocation of nitrogen.
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A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency.
Canopy position has a profound effect on soybean seed composition
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