Gen om e d iver si ty

Research Report
Project area Analysis of Growth and Metabolism during Ve-
getative Development 
central aims of the project area are the identification and charac-
terisation of factors influencing vegetative growth and heterosis 
in relation to plant metabolism. the superior features of the Ara-
bidopsis model system are used to identify at the molecular level 
loci causing variation in growth and metabolite contents. Growth 
related parameters and metabolic content were recorded in large 
genotyped populations of recombinant inbred lines (RiL), intro-
gression lines (iL), collections of accessions, and test crosses (tcs) 
for QtL analyses. currently, growth (biomass) heterosis QtL are 
fine-mapped, and candidate genes for heterotic biomass, tyro-
sine, urea, and fumarate contents are under investigation.
ongoing and future analyses focus on the verification of candi-
date genes and their functional analyses (qRt-PcR, Rna-Seq), 
which will include temporally and spatially highly resolved ex-
pression and metabolome profiling for primary candidates. an 
important aspect is the transfer of the knowledge on heterosis 
and novel concepts gained in Arabidopsis to crop species such 
as maize and rapeseed and comparative analyses. 
Identification and analysis of growth and growth heterosis 
candidate genes
F1 hybrids between accessions c24 and col-0 show strong he-
terosis for early biomass accumulation due to effects on seed-
ling establishment (Meyer et al. 2012). using QtL mapping ana-
lyses in RiLs and iLs, the strongest QtL was fine-mapped to 14 
genes at the top of chromosome iV (Meyer et al. 2010). Parental 
accessions c24 and col-0 were transformed with single genes 
or cosmids spanning the QtL region (h.-J. Jeon, R.c. Meyer, un-
published results). Lines were phenotyped as homozygous t3 
or segregating t2 using the automated plant phenotyping sys-
Research Group: Heterosis
head:  Prof. thomas altmann
Scientists
IPK financed
altschmied, Lothar, dr.
borisjuk, Lioudmilla, dr. 
brandt, Ronny (0,50/1,00, since 01.10.2012)
Fuchs, Johannes (0,50, 01.08.-31.08.2013)
Jeon, hea-Jung (0,50, since 01.10.2013)
Meyer, Rhonda, dr. 
Radchuk, Ruslana, dr. (01.04.-30.06.2012)
Riewe, david, dr. 
Seyfarth, Monique (0,50/0,25, till 31.12.2012)
Grant Positions
arana ceballos, Fernando, dr. (dFG, till 14.07.2012)
Fuchs, Johannes (0,50 industry, till 31.01.2013; 0,50 bMbF/
dPPn, 01.02.-31.07.2013)
Gryczka, corina, dr. (bMbF, till 31.03.2012)
heinzel, nicolas, dr. (industry)
Junker, astrid, dr. (0,50 eu, 01.08.2012-31.10.2013; 0,50/1,00 
bMbF/dPPn, since 01.11.2012)
könig, christina (0,50 dFG, since 15.09.2012)
Munz, eberhard (0,50 dFG, since 01.06.2012)
Muraya, Moses Mahugu (bMbF)
Radchuk, Volodymyr, dr. (industry, since 01.09.2013)
Radchuk, Ruslana, dr. (0,50 industry, till 31.03.2012)
Rolletschek, hardy, dr. (industry, till 31.01.2013; aiF/bMWi, 
since 01.02.2013)
Rosso, Mario, dr. (bMbF, till 31.03.2013; bMbF/dPPn, since 
01.04.2013)
Seyfarth, Monique (0,50 Saxony-anhalt, till 30.04.2012)
Shi, Rongli, dr. (0,75/1,00 dFG, till 30.09.2013; bMbF/dPPn, 
since 01.10.2013)
tschiersch, henning, dr. (bMbF, till 30.04.2012; 1,00/0,50 indus-
try, till 30.11.2012; 0,50 bMbF/dPPn, since 01.06.2013)
Weigelt-Fischer, kathleen (bMbF, till 31.03.2013; bMbF/dPPn, 
since 01.07.2013)
Visiting Scientists/Scholars
ernst, Michaela, dr. (self-financed, till 31.05.2012)
Jeon, hea-Jung (korean Government, till 26.09.2013)
Muscolo, adele (ePPn, 15.09.-02.11.2013)
Pawelkowicz, Magdalena (ePPn, 01.06.-30.06.2013)
Seifert, Michael, dr. (self-financed, 01.01.-28.02.2013)
Sotak, Miro (self-financed, 18.11.-14.12.2013)
Goals
With the major aim of identifying factors controlling plant per-
formance characteristics, two complementary research areas 
are addressed within the group: (i) Genetic/genomic approa-

Abteilung Molekulare Genetik/
Department of Molecular Genetics
92
seed morphology. these data are now used to build multi-trait 
QtL analyses to increase the power to detect small effect QtL 
(d. knoch, J. koppolu, d. Riewe, R.c. Meyer, R. Schmidt, unpub-
lished results). Future plans include to map the seed lipidomic 
fraction of metabolites and to extent the approach to genome-
wide studies using hundreds of Arabidopsis accessions. 
Analysis and prediction of performance features in crop 
plants
an important aspect is the transfer of the knowledge on hetero-
sis gained in Arabidopsis to crop species such as maize and rape-
seed. of particular interest in this context is the prediction of 
heterosis using parental data: SnPs, structural genome variation 
(PaV/cnV), metabolite profiles, transcript profiles, and phenoty-
pic measures. Furthermore, we are evaluating the potential hy-
brid advantages (heterosis) under varying environmental con-
ditions to improve plant performance under natural conditions.
in the frame of the Gabi-eneRGY cooperation project projects 
(jointly with a. Melchinger, university of hohenheim; L. Willmit-
zer and M. Stitt, MPi-MP Golm; J. Selbig, Potsdam university; M. 
ouzunova, kWS einbeck; and their co-workers) a panel of 289 
diverse maize dent inbreds were genotyped using the maize 
50k SnP array and were characterized for agronomic traits and 
metabolite profiles and a subset of 92 inbreds and testcrosses 
thereof (selected after initial analysis of the entire population) 
has been characterized for vegetative growth performance un-
der controlled (glass house) conditions, for metabolite compo-
sition, and for transcript profiles (M. ernst, c. Gryczka, S. Friedel, 
unpublished data). using field performance data of testcrosses 
the joint analysis revealed that the parental SnP and metabolite 
data contain very substantial information useful for prediction 
of the general combining ability of the inbreds (Riedelsheimer 
et al. 2012a). Furthermore, correlation of metabolite contents 
with expression of agronomic traits and association mapping of 
QtL affecting metabolite levels highlighted individual metabo-
lic pathways such as lignin precursor biosynthesis to contribute 
to overall plant performance, e.g. dry matter yield formation 
(Riedelsheimer et al. 2012b). array-based comparative genomic 
hybridisation (acGh) analyses performed on 34 maize inbred 
lines revealed an extraordinary high level of copy number va-
riation (cnV) or presence/absence variation (PaV) of genomic 
segments (M. Muraya, M. Seiffert, unpublished data). Within the 
PLant-kbbe cornFed cooperation projects (jointly with a. Mel-
chinger, university of hohenheim; a. charcosset, inRa Moulon; 
d. brunel, cnG evry; c. Schön, tu München; M. ouzunova, kWS 
einbeck; and their co-workers) detailed genetic and phenoty-
pic characterisation of diverse collections of maize inbred lines 
(‘flint’, ‘dent’, and ‘tropical’ panels), dh lines and testcrosses the-
reof has been carried out. these and the aforementioned efforts 
have led to the accumulation of 50k SnP genotype data for a 
total of more than 1000 inbred lines and more than 2200 dh 
lines; the latter are arranged in a nested association mapping 
(naM) design (Rincent et al. 2012, bauer et al. 2013). a series of 
265 maize inbred lines were phenotyped for biomass accumu-
lation, water consumption and the collected data were used 
to determine water use efficiency (M. Muraya, unpublished 
results). the observed substantial genetic variation of this trait 
tem (Lemnatec). Leaf area was altered for two candidate genes, 
which are also involved in a regulatory network, indicating that 
the heterotic biomass (hb) QtL at the top of chromosome iV is a 
complex locus possibly involving more than one gene and epi-
stasis with other loci (h.-J. Jeon, R.c. Meyer, a. Junker, unpub-
lished results). characterization of t-dna k.o. mutants of genes 
in the support interval and testcrosses thereof is ongoing (k. 
Weigelt, d. Riewe, R.c. Meyer, unpublished data).
a biomass QtL on the top of chromosome iii that could be si-
mulated purely on the basis of the metabolic composition of 
the plants (Lisec et al. 2008) is suspected to be involved in cross 
talk between metabolism and growth control. to identify the 
causal gene(s), this bQtL was further fine-mapped in a targeted 
Ld mapping approach with 272 accessions. Significantly asso-
ciated SnPs cluster between 1.9 and 2.4 Mb resulting in identifi-
cation of nine candidate genes (M. Seyfarth, unpublished data). 
candidate gene t-dna k.o. mutants were phenotyped using 
the automated high-throughput plant phenotyping system 
(Lemnatec). candidates passing this test are then subjected to 
qRt-PcR and further phenotyping for validation (R.c. Meyer, c. 
klukas, d. knoch, unpublished results).
Characterization of genes corresponding to metabolite 
QTL in Arabidopsis thaliana and further investigation of 
growth – metabolism relations 
based on previous data of metabolite (m)QtL identified 
through gas chromatography-mass spectrometry (Gc-MS)-
based metabolic profiling of RiL and iL populations (Lisec et 
al. 2008), 30 candidate genes were selected for an initial ana-
lysis according to their proposed enzymatic role related to 15 
different metabolites affected by mQtL. effects on abundance 
of the corresponding metabolite were observed by t-dna k.o. 
mutations of 5 genes that were selected for further investiga-
tion using also tiLLinG mutants and dsRnai lines subjected to 
Gc/MS analyses (brotman et al. 2011; Riewe et al. 2012). 
characterisation of the tyrosine aminotransferase (tat) candi-
date gene At5g53970 revealed a high impact on tyrosine to to-
copherol conversion (Riewe et al. 2012). to investigate the im-
portance of other members of this poorly characterised gene 
family, effects on metabolism are studied in 14 independent 
t-dna k.o. lines for the seven members of the tat gene family, 
in tissues in which the mutated locus has a high native expres-
sion (eFP browser). analyses of polar components (tyrosine and 
related amino acids) indicated tat7 as the major contributor to 
tyrosine conversion in leaf and seed tissue. Most candidates 
show a significant effect on different groups of metabolites (M. 
heuermann, d. Riewe, unpublished results).
natural genetic variation of metabolism and growth in Arabidop  - 
sis was further studied in mature seeds of 402 RiLs using Gc-
MS and photometry. 319 metabolites and protein content were 
quantified and data used in QtL mapping. 573 mQtL and one 
protein QtL explained up to 92 % of the variance of particular 
metabolites. Pca revealed a clustering of samples, with Pca1 
mapping to the top of chromosome iV proximal to FRIGIDA, dis-
tinct from the major biomass heterosis QtL located upstream. 
correlation/FdR analysis including morphological traits dis-
played links between the metabolome, protein content and 

93
has been adapted for (a) quantification of 3d lipid gradients 
in living seeds and fruits of diverse species (borisjuk et al., Pro-
gress in Lipid Research 2013); (b) visualisation of in vivo com-
partmentation of metabolism in developing seeds (Rolletschek 
et al., Plant cell 2011; borisjuk et al., Plant cell 2013), and (c) 
discovery of the breathing space in seed (Verboven et al., new 
Phytologist 2013). the technology was further developed to 
serve a noninvasive platform for high throughput imaging of 
sub-millimetre seeds (Fuchs et al., Plant Physiology 2013) and 
the nMR approach was linked with state-of-the-art mass spec-
trometry (MaLdi) imaging to visualize numerous lipid species 
in seeds of cotton (horn et al., Plant cell 2013) and Camelina 
(horn et al., Plant Journal 2013). the research topic which are 
addressed using the established technology cover sink/source 
interactions (Radchuk et al., new Phytologist 2012), metabolic 
regulation in seeds, improvements in storage metabolism and 
stress resistance (oxygen deficiency, drought; Rolletschek 2012 
[habilitation], kalladan et al., Molecular breeding 2012). For this 
purpose, the imaging technologies are combined with traditio-
nal ‘omics’ analyses and metabolic modelling approaches (flux 
balance analysis). this integrative approach is used to study 
a range of crop species such as rapeseed, cotton, barley, pea, 
tobacco and soybean. Specific procedures, such as the nMR-
based quantification of seed sizes and composition as well as 
the assessment of changes in o
2
 and co
2
 levels are advanced 
into multiparallel / high throughput installations within the 
dPPn project to enable large scale analyses. these aformen-
tioned studies and research projects rely on intense collabo-
ration within iPk (n. von Wirén; F. Schreiber, a. börner) as well 
as external collaborations (P. Jakob at Würzburg university,  
J. Schwender at bnL/uSa, k.d. chapman at texas university/
uSa, t. neuberger at Penn State university/uSa). 
and preliminary results of genome-wide association tests indi-
cate the opportunity to map and identify genes affecting this 
agronomically important trait.
Upgrade of Plant Phenotyping Platforms
in the first phase of the bMbF-funded dPPn (German Plant Phe-
notyping network) project, which was started in october 2012, 
the existing plant phenotyping platforms (Lemnatec) of iPk are 
upgraded in order to provide new capabilities: Laser scanner 
systems are integrated, which support 3d reconstructions of 
individual plants and stands of plants and to derive more de-
tailed information on plant/stand architecture (and changes 
over time). new installations are being added for functional 
chlorophyll fluorescence in order to assess performance cha-
racteristics of the plant photosystem ii (such as maximum/
effective quantum yield, maximum efficiency, photochemical 
and non-photochemical quenching, etc., see Fig. 29). Further 
major upgrades are designed and developed to assess the root 
system of the plants simultaneously with capturing informa-
tion of the shoot. Furthermore, a network of online-sensors 
of environmental data (such as air temperature and humidity, 
irradiation, and co
2
 concentration as well as soil temperature, 
moisture and conductivity) and of plant data (such as organ 
temperature, light reflectance, and growth movements) is set 
up into the systems to support proper analyses of plant respon-
ses to environmental influences.
Project area Lipid Metabolism in Oil-storing Seeds 
to assess the concentration and the distribution of oil, of other 
storage compounds and to monitor the allocation of assimi-
lates in seeds, methods based on nuclear magnetic resonance 
(nMR) imaging, and computed tomography have been devel-
oped and are intensely used. nMR is a key methodology, which 
Fig. 29
False color representation of Photosystem ii electron transport rates of Arabidopsis thaliana plants of parents (col-0, parent 1; c24, parent 2) and F1 hybrids (col-0 x c24; c24 
x col-0) which display strong heterosis of early biomass accumulation (h. tschiersch).

Abteilung Molekulare Genetik/
Department of Molecular Genetics
94
cose pyrophosphorylase, reveal coordinated adjustment 
of c:n metabolism mediated by an overlapping metabolic-
hormonal control. Plant J. 69 (2012) 1077-1093.
h
orn
, P.J., a.R. k
orte
, P.b. n
eogi
, e. L
ove
, J. F
uchs
, k. S
trupat
, L. b
o
-
risjuk
, V. S
hulaev
, Y.J. L
ee
 & k.d. c
hapman
: Spatial mapping of 
lipids at cellular resolution in embryos of cotton. Plant cell 
24 (2012) 622-636.
h
uang
, X., S. e
ffgen
, R.c. M
eyer
, k. t
heres
 & M. k
oornneef
: epistatic 
natural allelic variation reveals a function of aGaMouS-
Like6 in axillary bud formation in Arabidopsis. Plant cell 24 
(2012) 2364-2379.
J
unker
, a. & h. b
äumlein
: Multifunctionality of the Lec1 transcrip-
tion factor during plant development. Plant Signal. behav. 
7 (2012) 1718-1720.
J
unker
, a., G. M
önke
, t. R
utten
, J. k
eilwagen
, M. S
eifert
, t.M. t
hi
, J.P. 
R
enou
, S. b
alzergue
, P. V
iehover
, u. h
ähnel
, J. L
udwig
-M
üller
, L. 
a
ltschmied
, u. c
onrad
, b. W
eisshaar
 & h. b
äumlein
: elongation-
related functions of LeaFY cotYLedon1 during the devel-
opment of Arabidopsis thaliana. Plant J. 71 (2012) 427-442.
J
unker
, a., h. R
ohn
, t. c
zauderna
, c. k
lukas
, a. h
artmann
 & F. S
chrei
-
ber
: creating interactive, web-based and data-enriched 
maps using the Systems biology Graphical notation. nature 
Protocols 7 (2012) 579-593.
J
unker
, a., h. R
ohn
 & F. S
chreiber
: Visual analysis of transcriptome 
data in the context of anatomical structures and biological 
networks. Front. Plant Sci. 3 (2012) 252.
J
unker
, a., a. S
orokin
, t. c
zauderna
, F. S
chreiber
 & a. M
azein
: Wiring dia-
grams in biology: towards the standardized representation of 
biological information. trends biotechnol. 30 (2012) 555-557.
k
aur
, h., k. S
haker
, n. h
einzel
, J. R
alph
, i. G
alis
 & i.t. b
aldwin
: en-
vironmental stresses of field growth allow cinnamyl alco-
hol dehydrogenase-deficient Nicotiana attenuata plants to 
compensate for their structural deficiencies. Plant Physiol. 
159 (2012) 1545-1570.
L
apin
, d., R.c. M
eyer
, h. t
akahashi
, u. b
echtold
 & G. 
van
 
den
 a
cker
-
veken
: broad spectrum resistance of Arabidopsis c24 to dow-
ny mildew is mediated by different combinations of isolate-
specific loci. new Phytol. 196 (2012) 1171-1181.
M
eyer
, R.c., h. W
itucka
-W
all
, M. b
echer
, a. b
lacha
, a. b
oudichevskaia
, 
P. d
örmann
, o. F
iehn
, S. F
riedel
, M. 
von
 k
orff
, J. L
isec
, M. M
el
-
zer
, d. R
epsilber
, R. S
chmidt
, M. S
cholz
, J. S
elbig
, L. W
illmitzer
 & 
t. a
ltmann
: heterosis manifestation during early Arabidop-
sis seedling development is characterized by intermediate 
gene expression and enhanced metabolic activity in the 
hybrids. Plant J. 71 (2012) 669-683.
M
önke
, G., M. S
eifert
, J. k
eilwagen
, M. M
ohr
, i. G
rosse
, u. h
ähnel
, a. J
un
-
ker
, b. W
eisshaar
, u. c
onrad
, h. b
äumlein
 & L. a
ltschmied
:  towards  
the identification and regulation of the Arabidopsis thaliana 
abi3-regulon. nucleic acids Res. 40 (2012) 8240-8254.
M
uraya
, M.M., h.h. G
eiger
, F. S
agnard
, L. t
oure
, P.c.S. t
raore
, S. t
ogola
, 
S. 
de
 V
illiers
 & h.k. P
arzies
: adaptive values of wild × cultivated 
sorghum (Sorghum bicolor (L.) Moench) hybrids in genera-
tions F
1
, F
2
, and F
3
. Genet. Resour. crop evol. 59 (2012) 83-93.
R
adchuk
, V., J. k
umlehn
, t. R
utten
, n. S
reenivasulu
, R. R
adchuk
, h. R
ol
-
letschek
, c. h
errfurth
, i. F
eussner
 & L. b
orisjuk
: Fertility in bar-
ley flowers depends on Jekyll functions in male and female 
sporophytes. new Phytol. 194 (2012) 142-157.
Technology Platform Nucleic Acids Analyses 
For the hiSeq2000 sequencer (illumina) acquired and installed 
at the end of 2011, basic library synthesis protocols (dna and 
Rna paired-end) have been established in cooperation with re-
search group Genome diversity (a. himmelbach) and used for 
in-house applications and cooperation with external partners 
(R. horbach, MLu halle; h. Flachowsky, Jki dresden-Pillnitz; F. 
ordon/d. Perovic, Jki Quedlinburg; M. Lenhard, university Pots-
dam; S. Wenkel, zMbP tübingen; e. cellarova, university kosiče, 
Slovak Republic). these basic capabilities were extended to 
dna mate-pair, genotyping by sequencing, and small Rna 
protocols, which can now routinely be applied. together with 
research group bioinformatics and information technology 
(d. Schüler, S. Flemming, M. Lange) the laboratory information 
man agement system (LiMS) was adapted to store relevant in-
formation of library synthesis and sequencing runs.
as an application example, cdna of six different tissues of a di -
pl oid,  sexual  Hypericum perforatum accession as well as genomic 
dna have been sequenced (illumina paired-end) in coopera-
tion with research groups experimental taxonomy (F. blattner) 
and Gene Regulation (h. bäumlein) and assembled. these data 
were used to improve the annotation of bac insert sequences 
representing parts of the Hypericum perforatum apospory 
locus (haPPY) and corresponding sexual loci which were 
previously analysed (using 454 sequencing) in cooperation with 
research group Genome diversity (a. himmelbach). the current 
assemblies are available through a (password protected) bLaSt 
server (research group bit, Scholz). Sequence annotation of the 
polyketide gene family (cooperation with L. beerhues, university 
braunschweig) helped to identify the chS gene contributing to 
the haPPY locus. currently the improvement of bac contigs in 
the haPPY locus is under way using mate-pair sequences.
Publications
Peer Reviewed Papers
2012
a
ndorf
, S., R.c. M
eyer
, J. S
elbig
, t. a
ltmann
 & d. R
epsilber
:  integra tion 
of a systems biological network analysis and QtL results 
for biomass heterosis in Arabidopsis thaliana. PLoS one 7 
(2012) e49951.
b
oggetti
, b., J. J
asik
, M. t
akamiya
, u. S
trähle
, a.M. R
eugels
 & J.a. c
am
-
pos
-o
rtega
: nbP, a zebrafish homolog of human kank3, is a 
novel numb interactor essential for epidermal integrity and 
neurulation. dev. biol. 365 (2012) 164-174.
b
orisjuk
,  L., h. R
olletschek
 & t. n
euberger
: Surveying the plant’s 
world by magnetic resonance imaging. Plant J. 70 (2012) 
129-146.
b
urkart
-W
aco
, d., c. J
osefsson
, b.R. d
ilkes
, n. k
ozloff
, o. t
örjek
, R. 
M
eyer
, t. a
ltmann
 & L. c
omai
: hybrid incompatibility in Ara-
bidopsis is determined by a multi-locus genetic network. 
Plant Physiol. 158 (2012) 801-812.
F
aix
, b., V. R
adchuk
, a. n
erlich
, c. h
ümmer
, R. R
adchuk
, R.J. n
eil
 e
mery
, 
h. k
eller
, k.P. G
ötz
, W. W
eschke
, P. G
eigenberger
 & h. W
eber
: bar-
ley grains, deficient in cytosolic small subunit of adP-glu-

95
a. c
harcosset
, o.c. M
artin
 & c.c. S
chön
: intraspecific variation 
of recombination rate in maize. Genome biol. 14 (2013) R103.
b
orisjuk
, L., t. n
euberger
, J. S
chwender
, n. h
einzel
, S. S
underhaus
, J. 
F
uchs
, J.o. h
ay
, h. t
schiersch
, h.P. b
raun
, P. d
enolf
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