epignetica y productividad de los cultivos

Available online at www.sciencedirect.com

Energy efficiency and energy homeostasis as geneticand epigenetic components of plant performance andcrop productivityMarc 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 confirmed 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, defined here as

energy efficiency, rather than respiration on its own, has a

major impact on the yield potential of a crop. Besides energy

efficiency, 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 efficiency and energy homeostasis have an epigenetic

component that can be directed and stabilized by artificial

selection (i.e. selective breeding). This novel approach offers

new opportunities to improve yield potential and stress

tolerance in a wide variety of crops.

Addresses1 Bayer BioScience N.V., 9052 Gent, Belgium2 Department of Plant Systems Biology, VIB, 9052 Gent, Belgium3 Department of Plant Biotechnology and Genetics, Ghent University,

9052 Gent, Belgium

Corresponding author: De Block, Marc ([email protected])

Current Opinion in Plant Biology 2011, 14:275–282

This review comes from a themed issue on

Physiology and metabolism

Edited by Ute Kramer and Anna Amtmann

Available online 14th March 2011

1369-5266/$ – see front matter

# 2011 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.pbi.2011.02.007

Crop yieldA complex trait is defined 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

www.sciencedirect.com

between genotype and phenotype. Crop yield is con-

sidered 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 breed-

ing, 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 specific 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 protec-

tion, 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 environ-

mental conditions change (Figure 1b).

This review will mainly focus on energy metabolism in

relation to plant performance and more specifically on the

maintenance of energy homeostasis and the improvement

of energy efficiency 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.


mailto:[email protected]

http://dx.doi.org/10.1016/j.pbi.2011.02.007

276 Physiology and metabolism

Figure 1

Current Opinion in Plant Biology

100

75

50

% y

ield

gro

wth

/ yi

eld

0

25

100

75

% energy

healthy

severedamage

death

damage

50

0

25

(a)

(b)

(c)

Water availability

actual yield

geneticimprovement

unadvoidablelosses

actualcrop losses

IIyield gap

yield response tocrop protection

yield without crop protectionattainable yieldyield potential

actual

Drought Flooding

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 irre-

versible causing the death of the plant cell and, ulti-

mately, of the whole plant. Besides the ‘single-gene’

approaches that have been evaluated to maintain energy

homeostasis and to improve energy efficiency, we will

highlight the more recent and, perhaps more promising,


‘epigenomic’ strategies to improve the energy status of

plants.

The central role of NAD+ in energyhomeostasisThat energy metabolism has a great impact on plant pro-

ductivity 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, caus-

ing a negative energy balance. When the energy level drops

below a certain threshold, growth will stop, damage will

accumulate and, finally, the organism will die (Figure 1c).

Although photosynthesis is the main driver of plant pro-

ductivity, it is ultimately the cellular respiration (glycolysis,

citrate cycle, and mitochondrial electron transport) that

converts the fixed carbon into energy used for growth

and maintenance. In these energy flows, 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 path-

ways [6,7]. The networks controlled by NAD+, with the

main focus on energy metabolism, are schematically pre-

sented 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(ADP-

ribose) polymerases (PARPs) are induced. PARPs synthes-

ize from NAD+ large negatively charged chains of ADP-

ribose on mainly nuclear proteins as histones and transcrip-

tion factors by which their properties are changed. In this

process large amounts of NAD+ are metabolized what

finally 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 efficient than the de novo synthesis from

aspartate. Indeed, Arabidopsis lines overexpressing genes

from the NAD+ salvage pathway [12,13�] or the ADP-

Ribose/NADH pyrophosphohydrolases NUDX2 [14��]and NUDX7 [15] result in plants that maintain their

NAD+ and ATP levels and have an increased stress toler-

ance. The enzymes NUDX2 and NUDX7 metabolize the

ADP-ribose monomers derived from the breakdown

by poly(ADP-ribose) glycohydrolase (PARG) of the


Energy efficiency and energy homeostasis as genetic and epigenetic components De Block and Van Lijsebettens 277

Figure 2


AMPRibose-5-P

ADP-ribosylcyclase Ca2+

signalingcADP-ribose

fermentation TCAcycle

glycolysis

redox reactions

histonedeacetylation

NamAcetyl-ADP-ribose

AMPNMN

aspartate

Namde novo

synthesis

NAD

+ dip

hosp

hata

ses

Sirt

uins

Saivage pathway

growth, maintenance, ...

mitochondrialelectron transport

ABAstress

tolerance

ATP

NADH

NAD+

NADP+Oxidative pentose phosphate pathway

Photosynthesis....

ADP-ribose

poly(ADP-ribosyl)ation

NUDX2NUDX7

PARG

PARP

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 flexible

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 cADP-

ribose [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 deficiency occurs [17].

High-yielding crop varieties are energyefficientAlready 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��],


but this correlation is not absolute and other factors are

probably involved as well [21–23]. 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 sufficient 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), defined as energy efficiency, that deter-

mined plant performance and plant productivity. On

the basis of this principle, the potential yield of canola

could be increased by selecting for high-energy effi-

ciency. The link between potential yield and energy

efficiency was further supported by crosses between

female and male breeding lines of canola of which the

energy efficiency 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-efficient lines and hybrids were more



Figure 3

(a) (b)Matrix Intermembrane

spaceMatrix Intermembrane

spaceCitric acid cycle Citric acid cycle

Succinate

Fumarate

Succinate

Fumarate

NAD(P)H NAD(P)H

Photorespiration Photorespiration

FADH2

NADH

Complex I H+ H+

H+

H+

H+ H+

H+

H+

H+

ADP + PI

ATPH+

ADP + PI

ATP

Complex II

Complex III

Complex IV

Complex V

UQ

Complex I

Complex II

Complex III

Complex IV

Complex V

UQ

Ext1

Ext2Int1

Ext1

Ext2Int1

NAD+

NADH

NAD+

NAD(P)+

NAD(P)H

NAD(P)+NAD(P)+

2 e- 2 e-

2 e-

2 e-

2 e-

2 e-

2 e-

2 e-

2 e-

2 e-

Alternativeoxidase

Cyt C Cyt C

FAD+

FADH2

FAD+

2H+ + ½O2

½O2

H2O

NAD(P)H

NAD(P)+

2 e- Alternativeoxidase

2H+ + ½O2

H2O

H2O

2 e-

½O2

H2O


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 field con-

ditions. In this specific case, respiration and energy effi-

ciency correlated with mitochondrial complex I activity

(Figure 3). The low-respiring lines had a high complex I

activity and an efficient 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 high-

respiring lines that had a low complex I activity. In these

lines, electrons were mainly shuttled into the mitochon-

drial 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 influences other processes (networks) such as ascor-

bate synthesis. The last enzyme of the ascorbate syn-

thesis, 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


to a high ascorbate synthesis [26,27]. A low respiration

generates also fewer radicals. Thus, low radical pro-

duction, high ascorbate content, and improved energy

homeostasis together optimize overall plant performance.

Metabolism and epigenetic flexibilityIn nucleosomes, the DNA is wrapped around dimers of

histone H2A, H2B, H3, and H4. DNA methylation and

N-terminal histone modifications, such as acetylation,

methylation, and ubiquitination, regulate the accessibil-

ity of the DNA for RNAPII-mediated transcription and

either repress or activate gene expression. The availabil-

ity 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 specific loci

and is described as epigenetic flexibility. 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 ATP–citrate lyase and the

availability of glucose [28��]. The Sir2 histone deacety-

lase is responsive to metabolic cues because it requires

NAD+ for its deacetylase activity [29]. Reduced DNA



Figure 4

Selfing

Energy efficiency

Fre

qu

ency

Fre

qu

ency


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.

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 methyltransfer-

ases 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 muta-

tional interference with the SAM synthesis induced

hypomethylation, release of silenced transgenes in

tobacco (Nicotiana tabacum) [38], and caused the simul-

taneous removal of both DNA and histone methylations

in silenced Arabidopsis lines [39��], stressing the import-

ance of metabolite availability for epigenetic gene regu-

lation. Thus, epigenetic flexibility 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 efficiency

has been demonstrated to possess an epigenetic com-

ponent that can be selected for [20��]. Individuals of

isogenically doubled haploid canola populations are

genetically identical, but the distribution of their energy

efficiency 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, methy-

lome, and histone modifications in which respiration

varied by up to 70% and yield by up to 40%, suggesting

a huge potential of epigenetics for breeding.

Feasibility of epigenetic breedingDuring development, the epigenetic flexibility occurs at

specific 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 toadflax) [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 [42–44]. 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 Koval-

chuk 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 fitness at 308C than the progenies from the

untreated controls, suggesting a memory for the tempera-

ture treatment [48]. Indeed, the stress-induced loss of gene


silencing at a transgene gene locus had been linked to

altered histone modifications, while DNA methylation

remained unchanged [49�]. The cooperation of multiple

chromatin modifications, i.e. histone methylation and

DNA methylation, at specific 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 transgenera-

tional 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



wild type. Variation in complex traits, such as flowering

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 defined by multiple epial-

leles 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 modifications [20��] (our unpublished data). The

extreme phenotypic differences and the high transge-

nerational stability had been obtained by applying a

recurrent selection over three to five generations. Each

selection cycle had been accomplished on individual

plants derived from the progeny of the previous selection

(Figure 4). Moreover, the epigenetic ‘energy efficiency’

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 findings

open new possibilities for improving the yield potential

of both open-pollinating lines and hybrids.

ConclusionsEnergy efficiency and homeostasis are integral parts of

yield. Optimization of energy metabolism allows increas-

ing 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 first 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 back-

grounds. Most single-gene technologies are expected to

fail when transferred to elite breeding material that has

already been selected for good performance under various

field 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.


AcknowledgementsWe thank Martine De Cock for help in preparing the manuscript. This workis supported by the Agency for Innovation by Science and Technology inFlanders (IWT, O&O project ‘EpiTrait’).

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