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Proc Natl Acad Sci U S A. Nov 24, 2009; 106(47): 20109–20114.
Published online Nov 6, 2009. doi:  10.1073/pnas.0908755106
PMCID: PMC2774259
Plant Biology

Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield

Abstract

Quantitative traits, such as size and weight in animals and seed yield in plants, are distributed normally, even within a population of genetically identical individuals. For example, in plants, various factors, such as local soil quality, microclimate, and sowing depth, affect growth differences among individual plants of isogenic populations. Besides these physical factors, also epigenetic components contribute to differences in growth and yield. The network that regulates crop yield is still not well understood. Although this network is expected to have epigenetic elements, it is completely unclear whether it would be possible to shape the epigenome to increase crop yield. Here we show that energy use efficiency is an important factor in determining seed yield in canola (Brassica napus) and that it can be selected artificially through an epigenetic feature. From an isogenic canola population of which the individual plants and their self-fertilized progenies were recursively selected for respiration intensity, populations with distinct physiological and agronomical characteristics could be generated. These populations were found to be genetically identical, but epigenetically different. Furthermore, both the DNA methylation patterns as well as the agronomical and physiological characteristics of the selected lines were heritable. Hybrids derived from parent lines selected for high energy use efficiencies had a 5% yield increase on top of heterosis. Our results demonstrate that artificial selection allows the increase of the yield potential by selecting populations with particular epigenomic states.

Keywords: Brassica napus, epigenome

The variability of a quantitative trait depends on genetic, epigenetic, and environmental factors as well as on their mutual interactions. Particularly, plants that cannot escape their environment have to adapt quickly. The importance of the epigenome in both short-term and long-term adaptations to stress was demonstrated by the elevated recombination frequencies in the offsprings of Arabidopsis thaliana populations that had been stressed with UV-B radiation or flagellin (1). These increased levels of recombination could be transmitted to successive generations that had not been exposed to the stress.

Although there is no direct proof that recurrent selection can direct the epigenetic component of a quantitative trait, previous data suggest that it might be possible (2, 3). From a population obtained by a cross between two inbred flour beetles (Tribolium casteneum) with an average pupa weight of 2,400 μg, a population with an average pupa weight of 5,800 μg could be selected by continuous inbreeding for 120 generations (2, 3). Surprisingly, such a genetic variability was maintained over so many generations of inbreeding. Most probably, at a certain stage of the selection process, not genetic, but epigenetic variability, was dealt with, as further supported by identical experiments starting with one of the inbred lines homozygous for the genes affecting pupa weight (4).

For a long time, the epigenome has been believed to reset during meiosis. However, in numerous cases, epigenetic changes can be maintained during many generations. In plants, the flower-specific hypermethylated superman and agamous epialleles and the disease resistance hypomethylated late-flowering and ball epialleles are well-known (57). In fact, the transgenerational epigenetic inheritance holds true for many taxa, including animals, fungi, and bacteria (8). Recently, in Arabidopsis, epialleles across the genome were shown to be stably transmitted over consecutive generations (9).

One of the most complex quantitative traits in plants is yield because it is determined by many interacting components. Although a major subject in plant research for many decennia, the understanding of the biological network controlling yield is only poorly understood. Here we show that in canola (Brassica napus), energy use efficiency (EUE) is a major yield component with an epigenetic feature that can be directed by recursive selection. The shaping of the epigenome allows the increase of seed yield in both open-pollinating lines and hybrids.

Results and Discussion

Selection of Sublines from an Isogenic Line Based on Respiration.

A positive correlation between yield and low cellular respiration rates has been demonstrated in canola, Lolium perenne, tomato (Solanum esculentum), and cucumber (Cucumis sativus) (1016). Based on the published experimental concept (24), an artificial bidirectional selection procedure was established in canola for high and low cellular respiration rates. We started from an isogenic doubled haploid line to eliminate variation due to differences at the genetic level. As schematically presented (Fig. 1), out of 200 seedlings from the doubled haploid population “Simon,” seedlings with the lowest and highest cellular respiration were identified and retained. The two plants with the highest and lowest respiration were withheld for seed production by self-fertilization. These two populations were the starting material for four additional rounds of selection for sublines with high and low respiration rates. Seven lines were generated: four lines with lower (LR76, LR76-crashed, LR77, and LR79) and three with higher (HR80, HR82, and HR83) respiration than that of the control from which the selection had been initiated (Fig. 2). The “LR76-crashed” line was derived from a further selection for low respiration starting from the line LR76. The respiration of line LR76-crashed dropped below a critical threshold, resulting in reduced vigor (see below). At the individual plant level, the variation was high in the high-respiration lines [for instance, line HR82 with 125 ± 74% (mean ± standard deviation) compared to the control], and minimal in the low-respiration lines (for instance, line LR76 with 90 ± 18% versus the control). The high variation in respiration found between individual plants in the high-respiration lines is mainly due to the exponential increase of respiration once a certain threshold is passed (1.5 times the average respiration of the control line). This results in plants having up to six times higher respiration than the average respiration of the control line (supporting information (SI) Fig. S1). The high efficiency with which these lines were generated (from only 200 seedlings per selection cycle) suggests that no mutations are involved. Extensive amplified fragment-length polymorphism (AFLP) analyses did not identify differences between these lines and the control, except for the very high-respiration line HR83. The highest respiring plants of line HR83 have an abnormal development, are both male and female sterile, and have often chromosome deletions and inversions. Therefore, HR83 was not retained. Also the line LR79 was omitted in further analyses because its respiration was close to that of the control (97%).

Fig. 1.
Artificial selection for respiration and EUE in canola. The selection was initiated from an isogenic doubled haploid line. Approximately five selected plants with the lowest and highest respiration were self-fertilized, and the progenies were tested for ...
Fig. 2.
Respiration of six selected populations versus the original starting population. The values were percent-normalized versus the average of the starting line “Simon.” Each node represents an individual plant. Each population contains approximately ...

The Selected Sublines Have a Distinct EUE.

High cellular respiration was expected to be linked to high energy production and vice versa. However, when the total amount of NAD(P)H, reflecting the energy content, was measured (Table 1), lines with a high and low respiration had a low and high NAD(P)H content, respectively, except for line “LR76-crashed.” When the ratio NAD(P)H versus respiration, defined as EUE, was calculated, respiration and EUE correlated inversely, except for line LR76-crashed (Table 1). Probably, the respiration in line LR76-crashed dropped below a critical threshold to maintain sufficient energy production.

Table 1.
Physiological and agronomical properties of selected canola lines (% normalized versus control)

Complex I Activity and Ascorbate Content Are High and Photorespiration Is Low in the Low-Respiration Sublines.

During the selection procedure, respiration was quantified by measuring the reduction of 2,3,5-triphenyltetrazolium chloride (TTC) of hypocotyl explants. TTC reduction occurs at the end of the mitochondrial respiratory chain at complex IV (17) and, therefore, reflects the total electron flow through the mitochondrial respiratory chain, including the alternative oxidative respiratory pathway. The inhibitor of the alternative oxidase SHAM inhibits the reduction of TTC. The electrons enter the mitochondrial electron transport chain through complex I, complex II, and the internal and external alternative NAD(P)H dehydrogenases. The activity of complex I, the main dehydrogenase, was measured in leaf 3 of control and selected lines (Table 1), and an inverse correlation with respiration and complex I activity was observed. Recently, l-galactono-1,4-lactone dehydrogenase, the last enzyme of the plant ascorbate biosynthesis pathway, has been found to associate with an 800-kDa subcomplex of complex I and to have an important function in the accumulation of complex I, because complex I does not accumulate in Arabidopsis null mutants (18, 19). This apparent interrelation between ascorbate biosynthesis and complex I prompted us to measure the ascorbate content in the leaves of the different lines (Table 1). The lines with the highest respiration and the lowest complex I activity had the lowest ascorbate content and inversely. In summary, these results suggest that lines with a high and low respiratory rate have a reduced and increased complex I content, respectively. The high-respiration lines resemble the cytoplasmic male-sterile II (cmsII) mutant of Nicotiana sylvestris that lacks the NAD7 subunit of complex I (2021). The csmII mutant has no complex I activity, but its respiration is still high due to the compensatory enhanced activity of complex IV (cytochrome oxidase) and, probably, an increased activity of the alternative NAD(P)H dehydrogenases to meet the ATP needs of the cells. Lines with a high complex I content are more efficient in producing ATP, resulting in a low respiratory rate.

In tobacco (Nicotiana tabacum) and cucumber (Cucumus sativus), the decreased complex I capacity resulted in an increase in photorespiration (16, 22). Similarly, we found that the high-respiration lines had a significantly increased photorespiration, while that of the low-respiration lines was strongly reduced (Table 1), implying that low respiration, but not too low (as in the LR76-crashed line), correlates with a favorable physiological state and high respiration with a less fitness.

Yield Is Correlated with EUE.

The specific characteristics of the physiological states hint at a high or low stress tolerance (Fig. S2) and field performance. The selected and control lines were tested for seed yield in field trials (five locations with three to six replications of 10 m2/line) for 3 years (Table 1). Low-respiration lines with a high EUE had on average up to 8% higher seed yield than that of the control, while on average the seed yield was reduced by up to 10% in high-respiration lines with a low EUE. In fields with moderate drought stress, the line with the highest EUE had a 20% higher yield than that of the control, while the seed yield of the line with the highest respiration and lowest EUE dropped by 20%. With a Pearson correlation of 0.96, EUE and yield were very strongly positively correlated.

The Selected Sublines Have Altered Global DNA Methylation and Histone Modification.

The fact that the lines with high and low respiration had been generated efficiently from an isogenic line and that, based on the AFLP results, the selected lines were indistinguishable, suggest that the distinct physiological characteristics of the lines have an epigenetic basis. Hence, differential cytosine methylation and overall histone acetylation and methylation were studied to explore the epigenetic changes at the molecular level. First, a methylation-sensitive AFLP (ms-AFLP) analysis with HpaII and MspI as methylation-sensitive restriction enzymes on genomic DNA of leaf 3 revealed distinct differences (≈0.3%) between the selected lines and the control “Simon” (Fig. S3). Remarkably, all differentially methylated fragments that were sequenced (110 in total) corresponded to coding sequences. The ms-AFLP patterns were specific for each line and were maintained throughout different self-fertilizations for at least eight generations. Secondly, to evaluate differences in global methylation, cytosine extension assays were carried out on genomic DNA of leaf 3 in the different lines. In this assay, by means of the methylation-sensitive HpaII and MspI enzymes, it is possible to incorporate a single [3H]-labeled dCTP, after which the incorporated dCTP activity can be measured. An increase in activity corresponds to a decrease in global methylation. In general, the genomic DNA of the selected lines was hypomethylated (Fig. 3B), but the hypomethylation was more prominent in the low-respiration lines, with line LR76-crashed, being the most hypomethylated.

Fig. 3.
Characterization of the histone modifications and quantification of the global methylation of the genomic DNA by the cytosine extension assay. (A) Histones prepared from leaf 3 of the control line “Simon” and selected sublines. Below the ...

The distinct physiological state of the lines was also reflected at the histone level of the chromatin (Fig. 3A). In general, in the selected lines, except for HR82, the methylation at lysine 9 (Lys-9) and Lys-27 of histone 3 and acetylation at Lys-8, Lys-12, and Lys-16 of histone 4 was lower than that of the control line. The low-respiration line LR76 and its progeny LR76-crashed had a similarly low histone methylation and acetylation, whereas in the high-respiration line HR80 and line HR82, which is less vigorous than line HR80, the histone methylation and acetylation was the lowest and similar to that of the control, respectively. Hence, each of the selected lines is characterized by a specific degree of methylation and acetylation of histones 3 and 4. However, this overall picture does not reflect the physiological properties of the lines. More in-depth studies, such as chromatin immunoprecipitation (ChIP) analyses, might reveal a possible relation between histone modifications, gene expression, and vigor. Artificial selection for altered respiration and EUE clearly results in overall changes in DNA methylation and histone modifications through the plasticity of the epigenome (23). Extensive ms-AFLP analyses showed that none of the DNA methylation patterns found in the selected lines corresponded with methylation patterns of individual plants from the original population, indicating that recurrent selection for altered respiration at the individual plant level allows the selection for genes with specific and stable methylation states and distinct phenotypes, as a consequence.

The Subline Specific Respiration Rate Is Transmitted in Self-Fertilized Seeds and Backcrosses.

From the approximately eight generations of seed upscalings in the greenhouse and 3 years of elaborate field trials, it became obvious that the epigenetic EUE component of the lines was stably inherited by self-fertilized siblings (Fig. S3). As already described for the epigenetic recombination component in Arabidopsis (1), the epigenetic respiration component of canola can be transmitted in reciprocal backcrosses with a nonselected control line. For example, in the high-respiration line HR82 and similarly in the low-respiration line LR77, the self-fertilized progeny and the backcrosses to the original “Simon” line with HR82 and LR77 as females and males resulted in progenies with 127%, 124%, and 128% respiration and with 89%, 91%, and 93% respiration versus the control, respectively. The epigenetic inheritance was also reflected in the largely conserved DNA methylation patterns in the crosses compared to those of the self-fertilized selected lines. The methylation sites that were not conserved had a strong tendency toward hypomethylation, independently from the direction of the cross.

The Epigenetic EUE Component Can Be Added on Top of Heterosis.

Although “Simon” is a rather good performing canola line, we wanted to investigate whether the epigenetic EUE component could increase yield in elite varieties and hybrids. To this end, we selected high EUE in the parental lines of a top-yielding canola hybrid. Both the female and male lines are doubled haploids, and for this, each parental line was isogenic. After three to four recurrent selections for high EUE, hybrids were made with the selected parental lines (Fig. S4). The yield in these hybrids was higher (102–106%) than that of the control hybrid of which the parental lines had not been selected. The physiological characteristics were similar to the high-EUE “Simon” sublines: decreased mitochondrial complex I activity, reduced photorespiration, and increased ascorbate, ATP, and NAD(P)H contents (Table S1). Also at the molecular level, the selected hybrids were distinct from the control. Besides the specific differences in global DNA methylation with hypermethylation and hypomethylation in the cotyledons and leaves of the selected hybrids, respectively (Fig. 3C), the transcription profiles as analyzed by cDNA-AFLP were very distinct from the control hybrid (Fig. S5).

Concluding Remarks.

Our results show that EUE is a distinct feature of plant vigor and yield and that it possesses an epigenetic component that can be directed by artificial selection. In other words, it is feasible to select for a complex trait solely based on the epigenetic component. The main difference with the selection used in classical breeding schemes is that it is not only done at the population, but primary, at the plant level and in a recursive manner. However, the underlying mechanism that stabilizes the distinct epigenetic states is not understood. Starting from an isogenic population composed of plants with a variable epigenome, subpopulations with at least a partially fixed epigenome can be selected rather efficiently. It becomes even more puzzling when, during plant development, the epigenome of the selected sublines changes in opposite ways versus the control. For example, in hybrids generated by crossing parental lines that have been selected for higher EUE, the total genomic DNA is hypermethylated in the cotyledons, while in the fourth leaf, the genomic DNA is hypomethylated versus the control hybrid (Fig. 3C). It has to be mentioned that we found in our selections for higher EUE subpopulations that in the first rounds of selection returned to their original state. Only by recurrent selection the higher EUE could be fixed. It is not unlikely that the epigenetic stabilization can be tracked down to the expression of specific miRNAs. We are testing this possibility by making an inventory of the small RNAs in the selected and control lines.

The “epigenetic EUE component” is stably inherited, allowing the creation of distinct isogenic sublines that can be used in breeding. Probably as importantly, these isogenic sublines with distinct yield characteristics have a low “genetic noise” and, therefore, are excellent material to study yield and EUE at the molecular level. Initial experiments with cDNA-AFLP show clear differences in transcription between the sublines (Fig. S5) and microarray experiments being carried out to obtain a broader picture. Making an inventory of the small RNAs of the sublines and ChIP experiments with differentially methylated and/or expressed genes will contribute to a better understanding of the relation between DNA methylation (as the discrepancy in DNA methylation between cotyledons and leaves in the hybrids), histone modifications, transcription, and the resulting phenotypes. The fact that the concept can be used to further improve yield in already top-performing hybrids open perspectives to go beyond heterosis.

The central role of plant mitochondria in energy metabolism and their involvement in biochemical pathways, such as photorespiration, amino acid biosynthesis, and maintenance of redox status, is conserved in most plant species. Indeed, ongoing experiments indicate that analogous selections for EUE can be applied in rice (Oryza sativa) and tomato (Solanum esculentum). The implementation of the “epigenetic” selection for EUE has the potential to increase yield in many crops and this will further contribute to a better knowledge of the epigenetic mechanism, especially in crops, for which the genomics tools are well developed.

Materials and Methods

Artificial Selection for Respiration and EUE.

Seedlings were grown in vitro for 2 weeks on agar in half-strength Murashige and Skoog medium supplemented with 2% sucrose. The shoot tips of the seedlings were placed on the medium for rooting, while five hypocotyl explants per seedling were cultured for 5 days on callus-inducing medium (Murashige and Skoog medium supplemented with 3% sucrose and 1 mg/L 2,4-dichlorophenoxyacetic acid, 0.25 mg/L α-naphthaleneacetic acid, and 1 mg/L 6-benzylaminopurine). Cellular respiration of the hypocotyl explants was measured. The rooted shoot tips of approximately five seedlings with the highest and lowest respiration were transferred to the greenhouse for seed production by self-fertilization. Both respiration and NAD(P)H content of approximately 35–40 seedlings of the obtained progenies were measured. Lines with the lowest and highest respiration and highest and lowest EUE, respectively, were retained. The next rounds of selections were done in one direction for low or high respiration in lines with the lowest and highest respiration, respectively (Fig. 1). Three to five rounds of selection were sufficient to generate lines with distinct respiration and EUE. The same protocol was used for the production of more EUE hybrids. The male-sterile female, the maintainer, and the male restorer lines were each selected for low respiration and high EUE. After three cycles, the male-sterile female and restorer were crossed to produce hybrid seeds (Fig. S4).

Physiological and Biochemical Assays.

Cellular respiration of hypocotyl explants was quantified by measuring the reduction of TTC as described (14). ATP and total NAD(P)H contents were quantified as described (24, 25). EUE was expressed as the ratio of the percent-normalized values versus the control of NAD(P)H content to the amount of reduced TTC. Ascorbate content and complex I activity were measured with the reflectometric ascorbic acid test (Merck) and the MitoProfile Dipstick Assay kit (MitoSciences), respectively. The photorespiration intensity was quantified in vitro by floating cotyledons or leaf pieces on ammonium-free medium containing 3–5 mg/L glufosinate, incubated for 24 h under continuous light (≈70 μmol m−2 s−1). The ammonium production was evaluated as described (26). Photorespiration was expressed as percentage produced ammonium versus the control.

Field Trials.

For the field trials, five locations with different (from sandy to loamy) soil qualities were used. Each location was subdivided in six plots per line. Each plot was 10 m2 in size, with different arrangements of the plots for each location. Yield was expressed as kg seed/plot.

Statistics.

Data were statistically analyzed by one-way ANOVA with Dunnett's posttest with the Prism version 5.00 (GraphPad Software).

Molecular Analyses.

Methylation-sensitive AFLP (27) was done with the restriction enzyme combinations EcoRI-MspI/HpaII. The methylation state of the total genomic DNA was quantified with the cytosine extension assay as described (28). In summary, genomic DNA was prepared from cotyledons, leaf 3, or leaf 4 and assayed with the Quant-iT dsDNA High-Sensitivity Assay kit (Invitrogen). Of 10 individual leaves per line, 150 ng were used for the cytosine extension assay and digested with a 10-fold excess of HpaII and MspI. After 24 h, again a 10-fold excess of the restriction enzymes was added for another 24-h incubation. After 48 h, the single-nucleotide extension reaction was done with the digested genomic DNA. Of the reaction mixture, 10 μL were spotted on DE81 Whatman filters and washed three times with phosphate buffer (0.5 M, pH 7.0). The radioactive incorporation was measured (cpm).

Analyses of Histone Modifications.

Histones were acid-extracted, separated in NuPAGE 4–12% Bis-Tris gel (Invitrogen), and subjected to a standard procedure for immunoblotting with anti-H4-acetyl-Lys-8, anti-H4-acetyl-Lys-12 antibodies (Millipore), and with anti-H3-dimethyl-Lys-9 and anti-H3-trimethyl-Lys-27 antibodies (kind gifts of Thomas Jenuwein, Max Planck-Institute of Immunobiology, Freiburg, Germany).

Supplementary Material

Supporting Information:

Acknowledgments.

We thank T. Jenuwein (Max Planck-Institute of Immunobiology, Freiburg, Germany) for providing the antibodies against anti-H3-dimethyl-Lys-9 and anti-H3-trimethyl-Lys-27 and Dr. Martine De Cock for help in preparing the manuscript. This work was supported by the Institute for the Promotion of Innovation by Science and Technology in Flanders, Belgium (Research and Development project “Phoenix”) and an Industrial Agreement for Training through Research (CIFRE) fellowship (to H.A.).

Footnotes

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/cgi/content/full/0908755106/DCSupplemental.

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