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ScienceDirect Can we learn from heterosis and epigenetics to improve photosynthesis? Sascha Offermann and Christoph Peterhansel Heterosis is the increase in fitness and yield of F1 hybrids derived from a cross between distantly related genotypes. The use of heterosis is one of the most successful crop breeding strategies, but the underlying molecular mechanisms are still poorly defined. There is ample evidence that heterosis is associated with increased rates of photosynthesis and recent analyses have shed light on the underlying biochemical principles. In parallel, the importance of epigenetic chromatin modifications in heterosis has now been established. The first direct links between epigenetic changes and improved photosynthesis have also been demonstrated. As epigenetic engineering is now possible, we discuss the feasibility of altering the epigenetic code to enhance photosynthesis. Addresses Leibniz-University Hannover, Institute of Botany, Herrenhaeuser Strasse 2, 30419 Hannover, Germany Corresponding author: Peterhansel, Christoph ([email protected])

Current Opinion in Plant Biology 2014, 19:105–110 This review comes from a themed issue on Physiology and metabolism Edited by Sarah O’Connor and Tom Brutnell

http://dx.doi.org/10.1016/j.pbi.2014.05.010 1369-5266/# 2014 Elsevier Ltd. All rights reserved.

Introduction Photosynthesis provides the primary energy and carbon input for plant growth. Improving photosynthesis has been identified as a key strategy for the production of crop plants with higher biomass and yield [1,2]. Molecular targets were identified by the study of bottlenecks of photosynthesis [3,4]. Approaches to overcome these bottlenecks were mostly based on the up-regulation or down-regulation of single genes [5]. In some cases, synthetic pathways were used to overcome limitations of the endogenous pathways [6]. The ongoing efforts to engineer features of C4 photosynthesis into C3 plants are a current example [7]. Some of the tested approaches resulted in higher photosynthesis and biomass in the laboratory, but none were successfully applied to the improvement of crop performance in the field so far. The number of known molecular targets for improvement www.sciencedirect.com

of photosynthesis is still very limited. In this review, we analyze whether we can learn from studies on heterosis about new targets for upregulation of photosynthesis and whether epigenetics can be the key to using this knowledge for crop improvement.

Evidence for higher photosynthesis in hybrids Hybridization of distantly related genomes of one species in F1 hybrids and allopolyploid lines are perhaps the most apparent examples of how a breeding approach can be applied to enhance biomass and improve yield [8,9]. The increased fitness of hybrids compared to their parents is referred to as hybrid vigor or heterosis [9]. The effects of heterosis are most apparent in the first generation of a wide cross. Thus, hybrids cannot be sexually propagated without losing heterosis [10]. The higher biomass of hybrids compared to their parents implies that they have a higher lifetime carbon gain. This higher carbon gain is often referred to as ‘increased photosynthesis’, but many factors may contribute to this trait. Figure 1 provides an overview of some mechanisms that can cause higher carbon gain of the plant. First, higher carbon gain might be simply based on larger or more leaves, that is a larger photosynthetic area. This has been reported from crops like maize [11] and sorghum [12], as well as in Arabidopsis. In the latter example, F1 hybrids of the accessions Columbia and C24 established larger photosynthetic areas very early in development [13,14]. The larger size of the leaves was collectively caused by an increased cell number and an increased size of individual cells [14]. Metabolite profiling revealed a higher metabolic activity of the hybrids at early growth stages [14]. In one of the studies, transcripts related to photosynthesis were overrepresented among the genes that were expressed at higher levels in the hybrid compared to the parents [13]. Although the hybrids did not show higher photosynthesis on a leaf area basis, treatment with Norflurazon, an inhibitor of carotenoid biosynthesis, abolished the growth advantage of the hybrid indicating that active photosynthesis was required for heterosis in this system [13]. In addition to a larger photosynthetic area, the same leaf area might be used for longer periods of photosynthesis, either due to delayed senescence, earlier appearance of leaves, or a later down-regulation of daily photosynthesis before dusk. Analysis of photosynthesis in flag leaves of a rice hybrid [15] or a wheat hybrid [16] revealed delayed senescence compared to the inbred parents’ flag leaves. Current Opinion in Plant Biology 2014, 19:105–110

106 Physiology and metabolism

Figure 1

Life time carbon gain

Prolonged photosynthetic period

Increased photosynthetic area

Increased photosynthesis per leaf area

delayed leaf senescence

earlier appearance of leaves

longer daily photosynthesis

larger leaves

more leaves

improved light capture

more photosynthetic units

higher sink capacity

less (photo)respiration

more gas exchange

higher chloroplast density

thicker leaves

higher stomatal conductance

higher Calvin cycle capacity

higher mesophyll conductance Current Opinion in Plant Biology

Summary of potential mechanisms resulting in higher lifetime carbon gain.

In contrast, Arabidopsis hybrids and allopolyploids showed changes in circadian gene regulation that resulted in stronger induction of evening genes including those involved in chlorophyll and starch biosynthesis. This in turn was not only associated with higher biomass, but also with accumulation of more chlorophyll, more soluble sugars and more starch [17]. A third contributor to higher carbon gain is increased photosynthesis per leaf area. In a comprehensive analysis of eight maize inbred lines and their hybrids from all possible one way crosses, highest heterosis was found for the photosynthetic rate per leaf area [18]. However, similar studies in rice indicated ambiguous results with either higher [19] or unaffected photosynthetic rates of the hybrid [20]. Again, there are several possible mechanisms that can cause an increase in photosynthesis per leaf area including better light capture, changes in leaf gas uptake, or an optimized biochemistry of carbon fixation (e.g. higher Calvin cycle activity), and most studies could not discriminate between these possibilities. In rice hybrids, decreased photorespiration might be part of an optimized biochemistry. An initial SAGE analysis of the rice super hybrid Lyp9 revealed that the transcript for serine: glyoxylate aminotransferase, a key enzyme of the photorespiratory pathway, was downregulated in the hybrid compared to both parents, whereas many other genes related to carbon and nitrogen fixation were upregulated [21]. A later proteomic study showed that three Current Opinion in Plant Biology 2014, 19:105–110

additional photorespiratory proteins were less abundant in the hybrid than in the parents [22]. These results suggested that this hybrid required less photorespiratory proteins. A further characterization of the transcriptomes of three different rice hybrids including the Lyp9 genotype revealed that genes related to C4 metabolism were transcriptionally upregulated in all the three hybrids compared to their respective parents. This increase was also detectable on the enzyme activity level [23]. Results were most evident for the cytosolic isoform of phosphoenolpyruvate carboxylase, the chloroplastic isoform of pyruvate: Pi dikinase, and the chloroplastic isoform of malic enzyme. Even in the C4 plant maize, higher expression of some C4 genes was detected in the ear shoots of a hybrid compared to its parents [24]. Gas exchange experiments with the rice hybrids, albeit indicating both higher photosynthetic rates at light saturation [23] and higher light use efficiency [22] of the hybrids, did not reveal characteristics of C4 photosynthesis such as a clearly reduced CO2 compensation point. Thus, it remains to be shown whether upregulation of C4 enzymes provides any benefit for the plant and whether a C4-like CO2 concentrating mechanism in a single cell is active in these hybrids.

Evidence for an involvement of epigenetic processes and use for crop improvement There is now increasing evidence from genome-wide studies in hybrids and their parents that epigenetic mechanisms are an important element of heterosis (for www.sciencedirect.com

Heterosis, epigenetics and photosynthesis Offermann and Peterhansel 107

Box 1 Epigenetics Classical definitions described epigenetics as the science of changes in gene function that are not based on changes in the DNA sequence and that are persistent through mitosis or meiosis (reviewed in Ref. [39]). The emphasis of these definitions was on heritability. Work during the last 20 years on the role of chromatin in the control of gene expression resulted in a new conception of epigenetics that includes more transient alterations. In a 2007 Nature review, Adrian Bird broadened the definition to ‘structural adaptation of chromosomal regions so as to register, signal, or perpetuate altered activity states’ [40]. These structural adaptations comprise at least four different processes: 1. Chromatin remodeling: The ATP-dependent increase in nucleosome mobility. This includes sliding of nucleosomes, removal of nucleosomes or parts of nucleosomes from the DNA, or the replacement of core histones with histone variants. Chromatin remodeling is mostly associated with gene activation [41]. 2. DNA methylation: Methylation of cytosine (C) in DNA has been traditionally associated with gene inactivation, but this simple interpretation was questioned by genome-wide analyses that showed high DNA methylation also in highly active genes [29]. Different from animals that methylate C only in symmetric CG dinucleotide motifs, plants methylate C in all sequence contexts. Small RNAs are important in specifying DNA regions for C methylation (see 4). 3. Histone modification: Covalent modifications of histones preferentially in their N-terminal flexible domains that result in changes of the DNA–histone interaction or provide binding sites for other proteins such as transcription factors [42]. Methylation (Me) and acetylation (Ac) of lysine residues are most prominent examples. Acetylation of various lysines on histone H3 and H4 is mostly found on active genes, but the reading of the histone methylation code is more complex. Lysines can be monomethylated, di-methylated, or tri-methylated and the interpretation of the modification depends on the position, for example, trimethylation of lysine 4 on histone H3 (H3K4) is a marker for active chromatin regions, whereas dimethylation of H3K9 is found in inactive chromatin regions. 4. RNA-mediated changes in chromatin structure: Short chromatin-associated RNAs (approx. 24 bases) can control the formation of heterochromatin on transposons and repetitive DNA elements in the nucleus. RNA-directed DNA methylation (RdDM) provides a direct link between RNA binding and gene silencing [29,43]. Longer RNAs (>100 bases) have recently also been implicated in developmental gene regulation [44].

a current definition of epigenetics, (see Box 1 and Figure 2)). For example, systematic comparison of expression levels, DNA methylation and histone modifications revealed clear correlations between epigenetic modifications and altered transcript levels in rice hybrids [25] as well as Arabidopsis hybrids [26]. Further evidence came from a study of F1 hybrids between genetically similar Arabidopsis accessions which still resulted in strong heterosis [27]. This was unexpected because the degree of heterosis normally positively correlates with the genetic distance between the parents and interspecific hybrids generally show highest heterosis [8]. From small RNA abundances and DNA methylation profiles, it was concluded that a greater epigenetic distance rather than genetic distance was responsible for heterosis in this system [27]. One mechanism which might explain such www.sciencedirect.com

behavior is trans-chromosomal DNA methylation/ demethylation which alters one parental allele to the DNA methylation state of the other parent [26]. The heritable form of such allelic interaction is called paramutation and has also been shown to be controlled by DNA methylation in maize [28]. The general importance of DNA methylation for heterosis was recently demonstrated in a genome-wide study in Arabidopsis that revealed increased DNA methylation on both genes and transposons in hybrids relative to their parents. Inhibition of DNA methylation by 5-Azacytidine as well as disturbance of the RNA-dependent DNA methylation pathway abolished heterosis in the hybrids [29]. In accordance with this hypothesis, inbreeding depression, the reduced fitness of inbred plants compared to outcrosses, has also been associated with DNA methylation. Application of 5-Azacytidine increased light use efficiency and biomass of inbred Scabiosa plants, but not of the outbred control [30]. This suggests that DNA methylation was responsible for inbreeding depression. A direct link between epigenetic changes and higher photosynthesis was made in the Arabidopsis hybrids already mentioned above that showed changes in circadian gene regulation resulting in longer daily photosynthesis [17]. Here, deregulation of components of the central oscillator that caused the longer photosynthetic period could be directly attributed to changes in promoter histone modifications on the corresponding genes. If epigenetic changes were involved in the establishment of heterosis and perhaps in the increases of photosynthesis, then how could we use this knowledge for crop improvement? First of all, epigenetic changes in hybrids compared to parents could be used as markers to identify genes that are important for heterosis (Figure 3). Again, the study on heterosis and circadian gene control provides a good example. After identification of genes that were deregulated through epigenetic changes in the hybrid, classical genetics was used to mutate or overexpress these genes in inbred lines. The mutants showed phenotypes as predicted from the analysis of the hybrids [17]. In addition to using epigenetics as a tool for gene identification, specific manipulation of epigenetic marks is now feasible (Figure 3). In three independent studies, DNA or histone modifiers were targeted to promoters or enhancers using TALE technology [31,32,33]. This technology is based on the mechanisms governing recognition of plant promoters by bacterial avirulence proteins and allows the modular design of DNA-binding proteins with affinity to any given sequence [34]. In all three TALE studies, targeted alterations of epigenetic states were associated with changes in gene expression. Targeting of epigenetic modifiers using TALEs has so far only been tested in mammals and only with enzyme fusions that erase, but not write, epigenetic modifications. However, Current Opinion in Plant Biology 2014, 19:105–110

108 Physiology and metabolism

Figure 2

there is no reason to assume that the technology is not applicable in plant systems.

1.

2.

3.

Me C

4. RNA

Ac

Me

transcription

+

+/-

(-)

-

Current Opinion in Plant Biology

Epigenetic alterations of chromatin and their typical roles in control of transcription.

An important advantage of epigenetic manipulation would be that many genes could be regulated at the same time. A comparative analysis of C4 genes in maize in our lab revealed that a common histone modification code was used by these genes [35]. The same code was even applied in other C4 grasses suggesting that C4 genes were co-regulated by one or few transcription factors through conserved epigenetic modifications. Similar co-regulation of groups of genes related to specific gene programs by histone modifications was also observed in Arabidopsis for Polycomb protein EMF2 that regulates repression of flowering genes [36,37] as well as for histone deacetylase 15 that controls light response of photosynthetic genes [38].

Conclusion Heterosis is associated with increased photosynthesis, both if defined on a leaf area basis, and if defined more broadly as daily or life cycle carbon gain. Epigenetic changes of chromatin structure in hybrids play important roles in the establishment of heterosis. Hybrids can therefore guide our approaches to identify targets for improvement of photosynthesis. Engineering a hybrid-like state of epigenetic modifications into the genome of an inbred line could be a fascinating long-term goal of this work.

Figure 3

(1) Inbred parents

X

Acknowledgements (2) Heterotic F1 plant with increased photosynthesis

Work in the authors’ laboratories on epigenetics and photosynthesis is supported by the German research foundation (grants PE819/5-1, OF106/11, and GRK1798) and the European Union FP7 program (project 3to4; http://www.3to4.org).

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Heterosis, epigenetics and photosynthesis Offermann and Peterhansel 109

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Can we learn from heterosis and epigenetics to improve photosynthesis?

Heterosis is the increase in fitness and yield of F1 hybrids derived from a cross between distantly related genotypes. The use of heterosis is one of ...
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