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Energy efciency and energy homeostasis as genetic and epigenetic components of plant performance and crop productivity
Marc De Block1 and Mieke Van Lijsebettens2,3
The importance of energy metabolism in plant performance and plant productivity is conceptually well recognized. In the eighties, several independent studies in Lolium perenne (ryegrass), Zea mays (maize), and Festuca arundinacea (tall fescue) correlated low respiration rates with high yields. Similar reports in the nineties largely conrmed this correlation in Solanum lycopersicum (tomato) and Cucumis sativus (cucumber). However, selection for reduced respiration does not always result in high-yielding cultivars. Indeed, the ratio between energy content and respiration, dened here as energy efciency, rather than respiration on its own, has a major impact on the yield potential of a crop. Besides energy efciency, energy homeostasis, representing the balance between energy production and consumption in a changing environment, also contributes to an enhanced plant performance and this happens mainly through an increased stress tolerance. Although a few single gene approaches look promising, probably whole interacting networks have to be modulated, as is done by classical breeding, to improve the energy status of plants. Recent developments show that both energy efciency and energy homeostasis have an epigenetic component that can be directed and stabilized by articial selection (i.e. selective breeding). This novel approach offers new opportunities to improve yield potential and stress tolerance in a wide variety of crops.
Addresses 1 Bayer BioScience N.V., 9052 Gent, Belgium 2 Department of Plant Systems Biology, VIB, 9052 Gent, Belgium 3 Department of Plant Biotechnology and Genetics, Ghent University, 9052 Gent, Belgium Corresponding author: De Block, Marc (marc.deblock@bayer.com)

Current Opinion in Plant Biology 2011, 14:275282 This review comes from a themed issue on Physiology and metabolism mer and Anna Amtmann Edited by Ute Kra Available online 14th March 2011 1369-5266/$ see front matter # 2011 Elsevier Ltd. All rights reserved. DOI 10.1016/j.pbi.2011.02.007

between genotype and phenotype. Crop yield is considered as the most intricate plant trait because it consists of factors, such as seed set and seed size, that are complex traits as well. Besides the factors that directly contribute to yield, there are many yield-associated complex traits, such as abiotic stress tolerance. In agriculture and breeding, different types of yield are considered of which the most important are the potential, the attainable, and the actual yield (Figure 1a). The potential yield is the maximum yield a crop variety can reach under optimal growth and harvest conditions and is determined by the genetic and epigenetic constitutions of the crop. The main objective of breeding is to improve the potential yield by introducing new genetic resources. With the current agricultural practices, the potential yield can never be realized because there are always unavoidable losses, for instance, not every seed is harvested, resulting in the attainable yield. The record yields that are obtained at specic locations and years, approach the attainable yield. The most important yield losses are due to abiotic stresses and suboptimal culture conditions such as suboptimal soil composition. This gives the actual yield and corresponds to the harvest that varies from year to year. The difference between attainable and actual yield is called the yield gap. Many efforts are focused on closing this gap, mainly by breeding for stress tolerance or by adapting the agricultural practices, for instance by irrigation. It has to be remarked that without crop protection, such as spraying with herbicides, fungicides and insecticides yields would be extremely low [1] (Figure 1a). A valid strategy to increase overall plant performance and to narrow the yield gap is by broadening the growth optima for a wide range of environmental parameters, such as temperature, light intensity, water and nutrient availability. In such an enlarged window, growth, and yield will be less affected when the environmental conditions change (Figure 1b). This review will mainly focus on energy metabolism in relation to plant performance and more specically on the maintenance of energy homeostasis and the improvement of energy efciency to increase both the actual and potential yields. This strategy is based on the principle that a plant has to maintain a high energy level for an optimal growth and reproduction as is schematically depicted in Figure 1c. Decrease in energy content is only tolerated in a cell and in whole plants within a narrow window. Once the energy content drops below a certain level, damage occurs that is not (immediately) repaired.
Current Opinion in Plant Biology 2011, 14:275282

Crop yield
A complex trait is dened as a feature that is determined by a combination of multiple genetic, epigenetic, and environmental factors. These factors often interact in unpredictable ways resulting in a non-linear relation
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276 Physiology and metabolism

Figure 1

epigenomic strategies to improve the energy status of plants.

yield potential actual yield attainable yield yield without crop protection

(a)

The central role of NAD+ in energy homeostasis

That energy metabolism has a great impact on plant productivity and stress tolerance is well known [2,3,4]. A living organism has to maintain a high energy level to grow and to reproduce. Under stress conditions, energy consumption increases while energy production is often impaired, causing a negative energy balance. When the energy level drops below a certain threshold, growth will stop, damage will accumulate and, nally, the organism will die (Figure 1c). Although photosynthesis is the main driver of plant productivity, it is ultimately the cellular respiration (glycolysis, citrate cycle, and mitochondrial electron transport) that converts the xed carbon into energy used for growth and maintenance. In these energy ows, the common electron carrier is nicotinamide adenine dinucleotide (NAD+). Five adenosine triphosphates (ATPs) are needed for the de novo synthesis of NAD+ from aspartate and maximum three ATPs for its re-synthesis in the salvage pathway [4]. Overconsumption of NAD+ destabilizes the normal cell function and its resynthesis depletes the cellular ATP pool. A low energy level limits anabolism by which normal cell maintenance is disturbed, resulting in cell damage and, ultimately, in cell death. In addition to its main function in energy metabolism, the ratio of NAD+/ NADH regulates and drives many redox reactions [5]. An often overlooked but similarly important function of NAD+ and its metabolites is the interaction with signaling pathways [6,7]. The networks controlled by NAD+, with the main focus on energy metabolism, are schematically presented in Figure 2. For a normal functioning, the NAD+ content of cells is maintained at a rather constant level [8,9]. When plants are exposed to oxidative stress, poly(ADPribose) polymerases (PARPs) are induced. PARPs synthesize from NAD+ large negatively charged chains of ADPribose on mainly nuclear proteins as histones and transcription factors by which their properties are changed. In this process large amounts of NAD+ are metabolized what nally may result in cell death [10]. By reducing the (ADP-ribose) polymerase activity, energy homeostasis is maintained for a prolonged time under stress conditions, resulting in an improved stress tolerance as demonstrated in Arabidopsis thaliana and Brassica napus [10,11]. Energy homeostasis is also obtained when the NAD+ metabolites are recycled by the salvage pathway which is at least 40% more energy efcient than the de novo synthesis from aspartate. Indeed, Arabidopsis lines overexpressing genes from the NAD+ salvage pathway [12,13] or the ADPRibose/NADH pyrophosphohydrolases NUDX2 [14] and NUDX7 [15] result in plants that maintain their NAD+ and ATP levels and have an increased stress tolerance. The enzymes NUDX2 and NUDX7 metabolize the ADP-ribose monomers derived from the breakdown by poly(ADP-ribose) glycohydrolase (PARG) of the
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genetic improvement

100

unadvoidable losses

% yield

75

actual crop losses II yield gap

50
yield response to crop protection

25

(b)

growth / yield

Drought

Flooding

Water availability 100 healthy 75 % energy 50 severe damage 25 death 0

Current Opinion in Plant Biology

(c)

damage

Concepts in agriculture and breeding. (a) The different types of yield and the yield gap. (b) Effect of broadening the growth optimum for different environmental parameters on growth and yield. Stresses can be considered as extreme conditions that affect plant growth and plant health significantly. (c) Effect of energy status on plant health.

As energy content drops further, damage becomes irreversible causing the death of the plant cell and, ultimately, of the whole plant. Besides the single-gene approaches that have been evaluated to maintain energy homeostasis and to improve energy efciency, we will highlight the more recent and, perhaps more promising,
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Energy efficiency and energy homeostasis as genetic and epigenetic components De Block and Van Lijsebettens 277

Figure 2

AMP Ribose-5-P NUDX2 NUDX7 ADP-ribose PARG PARP poly(ADP-ribosyl)ation

NADP+

Oxidative pentose phosphate pathway Photosynthesis ....

NAD+

ADP-ribosyl cyclase

cADP-ribose

Ca2+ signaling

ABA

stress tolerance

D+ dip

aspartate

NA

Nam

de

v no

ho

os

th yn

Sirt

ha

Sa

es

is

tas

iva

uins

a ep

es

thw

ay

sp

redox reactions fermentation TCA cycle glycolysis mitochondrial electron transport

histone deacetylation AMP NMN Nam Acetyl-ADP-ribose

NADH
growth, maintenance, ...

ATP
Current Opinion in Plant Biology

Central role of NAD+ in energy metabolism (omitting photosynthesis). The blue areas cover NAD+ catabolism and signaling. The light green area covers NAD+ synthesis. The redox reactions are indicated in dark green. The bubblegum area corresponds to the energy-generating pathways. Nam, nicotinamide; NMN, nicotinamide mononucleotide (modified from [54]).

ADP-ribose polymers produced by PARP (Figure 2). In summary, improvement of the energy homeostasis reduces the net energy consumption when the plant is exposed to unfavorable conditions. This broadens the window of the growth optimum (Figure 1b), makes the plant more exible towards environmental conditions and allows the narrowing of the yield gap (Figure 1a). However, not only the energy content per se determines plant performance. A whole range of pathways is regulated by the concentration and ratios of the energy metabolites, i.e. NAD+, NADH, and their derivatives, such as cADPribose [6,7,16]. Another very important regulator of plant metabolism is the energy sensor SnRK1, a serine/threonine kinase that acts as master regulator of transcription when energy deciency occurs [17].

High-yielding crop varieties are energy efcient

Already for 30 years, in several crops, such as perennial ryegrass, tomato, and canola, reduced respiration has been found often to coincide with enhanced yield [18,19,20],
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but this correlation is not absolute and other factors are probably involved as well [2123]. In selected canola lines, the rate of respiration has been demonstrated to be inversely correlated with plant productivity [20]. However, respiration can also be too low and may not be sufcient to sustain energy production. This type of low respiring lines (20% lower respiration versus the control) had a reduced yield [20]. In fact, it was not the rate of respiration per se, but the ratio between energy content and respiration (both expressed as percent versus control line), dened as energy efciency, that determined plant performance and plant productivity. On the basis of this principle, the potential yield of canola could be increased by selecting for high-energy efciency. The link between potential yield and energy efciency was further supported by crosses between female and male breeding lines of canola of which the energy efciency and, consequently, the yield had been improved [20]. These crosses resulted in high-yielding hybrids, and the yield increase of the parental lines was added onto the heterosis effect. Besides the yield increase, the energy-efcient lines and hybrids were more
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278 Physiology and metabolism

Figure 3

(a)
Matrix
Citric acid cycle Photorespiration Succinate FADH2 Fumarate FAD+ NAD(P)H Int1 NAD(P)+ 2H+ + O2 2 eH 2O Complex III Cyt C O2 2 eH 2O ADP + PI H+ ATP Complex V H+ Complex IV H+ H+
Alternative oxidase

(b)
Intermembrane space
Complex I NAD+ 2 eComplex II 2e 2e
-

Matrix
Citric acid cycle Photorespiration Succinate FADH2 Fumarate FAD+ Complex II 2 eUQ 2 eInt1 2 eNADH Complex I NAD
+

Intermembrane space
H+

NADH H
+

2 e-

UQ 2 eExt1 Ext2 NAD(P)H NAD(P)H NAD(P)+ 2H+ + O2 2 eH2O

Alternative oxidase

Ext1 Ext2

NAD(P)H

NAD(P)+

NAD(P)

Complex III Cyt C O2 2e H 2O ADP + PI H+ ATP Complex V

-

H+

Complex IV

H+

H+

Current Opinion in Plant Biology

Intensity of the mitochondrial respiration by complex I activity. (a) Lines with a high complex I activity have an efficient ATP production and need a less intense mitochondrial electron transport, with a low respiration as a result. (b) When the complex I activity is low, the reverse is true: more electrons will be shuttled into the mitochondrial electron transport chain via complex II and the internal and external alternative NAD(P)H dehydrogenases (Int1, Ext1, and Ext2). Bypassing complex I produces much less ATP, and a more intense mitochondrial electron transport is needed (red arrows) for the production of the same amount of ATP. In other words, more electrons will pass complex IV, resulting in an increased respiration [24,25].

tolerant to various stresses, such as drought and ozone, and outperformed the controls under adverse eld conditions. In this specic case, respiration and energy efciency correlated with mitochondrial complex I activity (Figure 3). The low-respiring lines had a high complex I activity and an efcient ATP production and needed a lower rate of mitochondrial electron transport, with a reduced respiration as consequence, to meet the ATP demands of the cell. The reverse was true for the highrespiring lines that had a low complex I activity. In these lines, electrons were mainly shuttled into the mitochondrial electron transport chain via complex II and the alternative NAD(P)H dehydrogenases. By bypassing complex I, much (at least 30%) less ATP is produced; thus a higher rate of mitochondrial electron transport is needed to maintain ATP production. Consequently, more electrons will pass through complex IV, resulting in a higher respiration rate [24,25]. An altered complex I also inuences other processes (networks) such as ascorbate synthesis. The last enzyme of the ascorbate synthesis, L-galactono-1,4-lactone dehydrogenase is part of a subcomplex of complex I, linking complex I activity to ascorbate synthesis: a high complex I activity corresponds
Current Opinion in Plant Biology 2011, 14:275282

to a high ascorbate synthesis [26,27]. A low respiration generates also fewer radicals. Thus, low radical production, high ascorbate content, and improved energy homeostasis together optimize overall plant performance.

Metabolism and epigenetic exibility

In nucleosomes, the DNA is wrapped around dimers of histone H2A, H2B, H3, and H4. DNA methylation and N-terminal histone modications, such as acetylation, methylation, and ubiquitination, regulate the accessibility of the DNA for RNAPII-mediated transcription and either repress or activate gene expression. The availability of metabolites, such as the methyl donor, S-adenosyl methionine (SAM), acetyl CoA, and NAD+, is one of the factors that determine the epigenetic state at specic loci and is described as epigenetic exibility. Indeed, in mammalian cells, histone acetylation and gene expression in response to growth factor stimulation and during differentiation are regulated by the level of acetyl CoA that depends on the activity of ATPcitrate lyase and the availability of glucose [28]. The Sir2 histone deacetylase is responsive to metabolic cues because it requires NAD+ for its deacetylase activity [29]. Reduced DNA
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Energy efficiency and energy homeostasis as genetic and epigenetic components De Block and Van Lijsebettens 279

methylation of genes by limiting methyl donors in the diet can lead to their overexpression and result in aging pathologies [30]. Histone acetyl transferases, Sir2-related sirtuin deacetylases, histone, and DNA methyltransferases are conserved in plants [31,32,33]. Recent reports link sirtuin activity with metabolism/energy availability, chromatin status, and gene expression in the unicellular alga, Chlamydomonas reinhardii, Arabidopsis, and rice (Oryza sativa) [34,35,36,37]. Pharmacological or mutational interference with the SAM synthesis induced hypomethylation, release of silenced transgenes in tobacco (Nicotiana tabacum) [38], and caused the simultaneous removal of both DNA and histone methylations in silenced Arabidopsis lines [39], stressing the importance of metabolite availability for epigenetic gene regulation. Thus, epigenetic exibility is expected to correlate with nutrient availability and energy homeostasis in plants and to be modulated by metabolic pathways and environmental cues (Figure 2). Indeed, energy efciency has been demonstrated to possess an epigenetic component that can be selected for [20]. Individuals of isogenically doubled haploid canola populations are genetically identical, but the distribution of their energy efciency was normal and correlated with a distinct seed yield and stress tolerance. Recurrent selection without mutagenic treatment resulted in a range of epigenetic variants (Figure 4) with distinct transcriptome, methylome, and histone modications in which respiration varied by up to 70% and yield by up to 40%, suggesting a huge potential of epigenetics for breeding.

Figure 4

Frequency

Selfing

Feasibility of epigenetic breeding

During development, the epigenetic exibility occurs at specic alleles, switching gene expression states from active to the silent or vice versa. Intriguingly, epialleles with heritable activity states are known to be stabilized through different mechanisms, such as DNA methylation in Linaria vulgaris (common toadax) [40], paramutation in maize [41], or polyploidy-associated transcriptional gene silencing in Arabidopsis [39]. The epigenome is also modulated by environmental stimuli, such as light and stress [4244]. The mechanism by which an epigenetic state is stably transmitted to the next generation is still unknown, but several studies addressed this question in relation to stress research. In this issue, Boyko and Kovalchuk review the effects of mild stress on the epigenetic status, and Mirouze and Paszkowski focus on transposon mobility in response to stress and the consequences for genetic variation [45,46]. In Arabidopsis, certain types of stresses enhanced somatic homologous recombination for several generations even in the absence of stress and this so-called transgenerational memory of stress was suggested to be due to epigenetic mechanisms [47]. Both the F1 and F3 progenies of a heat-treated parental line showed a higher tness at 308C than the progenies from the untreated controls, suggesting a memory for the temperature treatment [48]. Indeed, the stress-induced loss of gene
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Frequency

Energy efficiency
Current Opinion in Plant Biology

Artificial recurrent selection for energy efficiency. The selection is applied to a subpopulation of approximately 200 plants from an isogenic line. The plant with the highest energy efficiency is selected, from which seed is produced by self-fertilization. The selection cycle for the plant with the highest energy efficiency is repeated starting from the seeds of the previously selected plant. Three to five rounds of selection are sufficient to generate stable lines with an improved energy efficiency.

silencing at a transgene gene locus had been linked to altered histone modications, while DNA methylation remained unchanged [49]. The cooperation of multiple chromatin modications, i.e. histone methylation and DNA methylation, at specic transgene or endogenous loci generated an unanticipated stability of epigenetic states and might be a mechanism for transgenerational stability [39]. The importance of DNA methylation in transgenerational stability of epigenetic states was demonstrated in epigenetic Recombinant Inbred Lines (epiRILs), derived from crosses between an Arabidopsis mutant in the DNA methylation pathway (ddm1) and its isogenic
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280 Physiology and metabolism

wild type. Variation in complex traits, such as owering time and plant height, heritable over at least eight generations, was noticed among the epiRILs and was linked to the stable inheritance of parental epialleles [50]. However, when the epiRILs were derived from a cross between another DNA methylation mutant, met1, and its corresponding wild type, an unexpectedly high frequency of non-parental methylation polymorphisms was observed besides stable parental epialleles [51]. Although MET1 and DDM1 are both responsible for the maintenance of the mCG methylation, MET1 has additional epigenetic functions [52], which might explain the de novo methylation patterns in the epiRILs compared to DDM1. Hence, complex traits have an epigenetic component that is dened by multiple epialleles and might represent a, thus far, unexplored basis of variation [50]. Remarkably, the epigenetic variants obtained by Hauben et al. [20] were stable for over eight generations with respect to phenotypes, methylome, transcriptome, and histone modications [20] (our unpublished data). The extreme phenotypic differences and the high transgenerational stability had been obtained by applying a recurrent selection over three to ve generations. Each selection cycle had been accomplished on individual plants derived from the progeny of the previous selection (Figure 4). Moreover, the epigenetic energy efciency component could be added on top of hybrid vigor. Altogether, the data indicated that the epigenome can be reshaped, stable epigenomic changes can be selected for and transgenerationally stabilized. These ndings open new possibilities for improving the yield potential of both open-pollinating lines and hybrids.

Acknowledgements
We thank Martine De Cock for help in preparing the manuscript. This work is supported by the Agency for Innovation by Science and Technology in Flanders (IWT, O&O project EpiTrait).

References and recommended reading

Papers of particular interest published within the period of review have been highlighted as:  of special interest  of outstanding interest 1. Lobell DB, Cassman KG, Field CB: Crop yield gaps: their importance, magnitudes, and causes. Annu Rev Environ Resour 2009, 34:179-204. Nunes-Nesi A, Carrari F, Lytovchenko A, Fernie AR: Enhancing crop yield in Solanaceous species through the genetic manipulation of energy metabolism. Biochem Soc Trans 2005, 33:1430-1434. Dobrota C: Energy dependent plant stress acclimation. Rev Environ Sci Biotechnol 2006, 5:243-251.

2.

3. 4. 

Hashida S-N, Takahashi H, Uchimyia H: The role of NAD biosynthesis in plant development and stress responses. Ann Bot 2009, 103:819-824. This review is complementary to the present article because it summarizes very well the physiological signicance of NAD+ and NADPH biosynthesis in plant development and stress tolerance. 5. 6. 7. Noctor G, De Paepe R, Foyer CH: Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 2007, 12:125-134. Hunt L, Lerner F, Ziegler M: NAD new roles in signalling and gene regulation in plants. New Phytol 2004, 163:31-44. Koch-Nolte F, Haag F, Guse AH, Lund F, Ziegler M: Emerging roles of NAD+ and its metabolites in cell signaling. Sci Signal 2009, 2:mr1. Titok VV, Rusinova OV, Khotyleva LV: Changes in nicotinamide coenzymes and adenylate energy charge in leaves of hybrid and parental tomato forms in an in vitro culture. Biol Plant 1995, 37:507-513. Wang G, Pichersky E: Nicotinamidase participates in the salvage pathway of NAD biosynthesis in Arabidopsis. Plant J 2007, 49:1020-1029.

8.

9.

Conclusions
Energy efciency and homeostasis are integral parts of yield. Optimization of energy metabolism allows increasing both the actual and the potential yields of crops. It is questionable whether complex traits, such as yield, can be improved by modifying the expression of only a few genes. Although, some rst successes had been obtained with single-gene approaches to improve, for instance, drought tolerance [53], most of these experiments were done in growth chambers and in restricted genetic backgrounds. Most single-gene technologies are expected to fail when transferred to elite breeding material that has already been selected for good performance under various eld conditions. Until now, most progress in germplasm improvement is still achieved by classical and molecular breeding methods that indirectly modulate networks by using whole-genome approaches. In this context, epigenetic breeding based on recurrent selection and stabilization of particular epigenetic states of genes, chromosomal regions, and whole genomes, offers new perspectives for engineering plant metabolism and improving complex traits.
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