Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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A MYB Triad Controls Primary and Phenylpropanoid Metabolites for Pollen Coat Patterning
Battat, Maor ; Eitan, Asa ; Rogachev, Ilana ; Hanhineva, Kati ; Fernie, Alisdair ; Tohge, Takayuki ; Beekwilder, Jules ; Aharoni, Asaph - \ 2019
Plant Physiology 180 (2019)1. - ISSN 0032-0889 - p. 87 - 108.

The pollen wall is a complex, durable structure essential for plant reproduction. A substantial portion of phenylpropanoids (e.g. flavonols) produced by pollen grain tapetal cells are deposited in the pollen wall. Transcriptional regulation of pollen wall formation has been studied extensively, and a specific regulatory mechanism for Arabidopsis (Arabidopsis thaliana) pollen flavonol biosynthesis has been postulated. Here, metabolome and transcriptome analyses of anthers from mutant and overexpression genotypes revealed that Arabidopsis MYB99, a putative ortholog of the petunia (Petunia hybrida) floral scent regulator ODORANT1 (ODO1), controls the exclusive production of tapetum diglycosylated flavonols and hydroxycinnamic acid amides. We discovered that MYB99 acts in a regulatory triad with MYB21 and MYB24, orthologs of emission of benzenoids I and II, which together with ODO1 coregulate petunia scent biosynthesis genes. Furthermore, promoter-activation assays showed that MYB99 directs precursor supply from the Calvin cycle and oxidative pentose-phosphate pathway in primary metabolism to phenylpropanoid biosynthesis by controlling TRANSKETOLASE2 expression. We provide a model depicting the relationship between the Arabidopsis MYB triad and structural genes from primary and phenylpropanoid metabolism and compare this mechanism with petunia scent control. The discovery of orthologous protein triads producing related secondary metabolites suggests that analogous regulatory modules exist in other plants and act to regulate various branches of the intricate phenylpropanoid pathway.

Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds
Nunes-Nesi, Adriano ; Alseekh, Saleh ; Oliveira Silva, Franklin Magnum de; Omranian, Nooshin ; Lichtenstein, Gabriel ; Mirnezhad, Mohammad ; González, Roman R.R. ; y Garcia, Julia Sabio ; Conte, Mariana ; Leiss, Kirsten A. ; Klinkhamer, Peter G.L. ; Nikoloski, Zoran ; Carrari, Fernando ; Fernie, Alisdair R. - \ 2019
Metabolomics 15 (2019)4. - ISSN 1573-3882
Leaf metabolism - Metabolite network - Metabolite QTL - Tomato

Introduction: To date, most studies of natural variation and metabolite quantitative trait loci (mQTL) in tomato have focused on fruit metabolism, leaving aside the identification of genomic regions involved in the regulation of leaf metabolism. Objective: This study was conducted to identify leaf mQTL in tomato and to assess the association of leaf metabolites and physiological traits with the metabolite levels from other tissues. Methods: The analysis of components of leaf metabolism was performed by phenotypying 76 tomato ILs with chromosome segments of the wild species Solanum pennellii in the genetic background of a cultivated tomato (S. lycopersicum) variety M82. The plants were cultivated in two different environments in independent years and samples were harvested from mature leaves of non-flowering plants at the middle of the light period. The non-targeted metabolite profiling was obtained by gas chromatography time-of-flight mass spectrometry (GC-TOF-MS). With the data set obtained in this study and already published metabolomics data from seed and fruit, we performed QTL mapping, heritability and correlation analyses. Results: Changes in metabolite contents were evident in the ILs that are potentially important with respect to stress responses and plant physiology. By analyzing the obtained data, we identified 42 positive and 76 negative mQTL involved in carbon and nitrogen metabolism. Conclusions: Overall, these findings allowed the identification of S. lycopersicum genome regions involved in the regulation of leaf primary carbon and nitrogen metabolism, as well as the association of leaf metabolites with metabolites from seeds and fruits.

Mapping the Arabidopsis Metabolic Landscape by Untargeted Metabolomics at Different Environmental Conditions
Wu, Si ; Tohge, Takayuki ; Cuadros-Inostroza, Álvaro ; Tong, Hao ; Tenenboim, Hezi ; Kooke, Rik ; Méret, Michaël ; Keurentjes, Joost B. ; Nikoloski, Zoran ; Fernie, Alisdair Robert ; Willmitzer, Lothar ; Brotman, Yariv - \ 2018
Molecular Plant 11 (2018)1. - ISSN 1674-2052 - p. 118 - 134.
Different environments - GWAS - Network analysis - Secondary metabolism - Untargeted metabolomics

Metabolic genome-wide association studies (mGWAS), whereupon metabolite levels are regarded as traits, can help unravel the genetic basis of metabolic networks. A total of 309 Arabidopsis accessions were grown under two independent environmental conditions (control and stress) and subjected to untargeted LC-MS-based metabolomic profiling; levels of the obtained hydrophilic metabolites were used in GWAS. Our two-condition-based GWAS for more than 3000 semi-polar metabolites resulted in the detection of 123 highly resolved metabolite quantitative trait loci (p ≤ 1.0E-08), 24.39% of which were environment-specific. Interestingly, differently from natural variation in Arabidopsis primary metabolites, which tends to be controlled by a large number of small-effect loci, we found several major large-effect loci alongside a vast number of small-effect loci controlling variation of secondary metabolites. The two-condition-based GWAS was followed by integration with network-derived metabolite-transcript correlations using a time-course stress experiment. Through this integrative approach, we selected 70 key candidate associations between structural genes and metabolites, and experimentally validated eight novel associations, two of them showing differential genetic regulation in the two environments studied. We demonstrate the power of combining large-scale untargeted metabolomics-based GWAS with time-course-derived networks both performed under different abiotic environments for identifying metabolite-gene associations, providing novel global insights into the metabolic landscape of Arabidopsis. By combining large-scale untargeted metabolomics-based GWAS and network analysis with environmental stress-driven perturbations of metabolic homeostasis, this system-wide study provides new global insights into the metabolic landscape of Arabidopsis, using a strategy that could readily be extended to other plant species.

De Novo Assembly of a New Solanum pennellii Accession Using Nanopore Sequencing
Schmidt, Maximilian H.W. ; Vogel, Alexander ; Denton, Alisandra K. ; Istace, Benjamin ; Wormit, Alexandra ; Geest, H.C. van de; Bolger, Marie E. ; Alseekh, Saleh ; Mass, Janina ; Pfaff, Christian ; Schurr, Ulrich ; Chetelat, Roger ; Maumus, Florian ; Aury, Jean-Mary ; Koren, Sergey ; Fernie, Alisdair Robert ; Zamir, Dani ; Bolger, Anthony ; Usadel, Björn - \ 2017
The Plant Cell 29 (2017)10. - ISSN 1040-4651 - p. 2336 - 2348.
Updates in nanopore technology have made it possible to obtain gigabases of sequence data. Prior to this, nanopore sequencing technology was mainly used to analyze microbial samples. Here, we describe the generation of a comprehensive nanopore sequencing data set with a median read length of 11,979 bp for a self-compatible accession of the wild tomato species Solanum pennellii. We describe the assembly of its genome to a contig N50 of 2.5 MB. The assembly pipeline comprised initial read correction with Canu and assembly with SMARTdenovo. The resulting raw nanopore-based de novo genome is structurally highly similar to that of the reference S. pennellii LA716 accession but has a high error rate and was rich in homopolymer deletions. After polishing the assembly with Illumina reads, we obtained an error rate of <0.02% when assessed versus the same Illumina data. We obtained a gene completeness of 96.53%, slightly surpassing that of the reference S. pennellii. Taken together, our data indicate that such long read sequencing data can be used to affordably sequence and assemble gigabase-sized plant genomes.
The Sexual Advantage of Looking, Smelling, and Tasting Good : The Metabolic Network that Produces Signals for Pollinators
Borghi, Monica ; Fernie, Alisdair R. ; Schiestl, Florian P. ; Bouwmeester, Harro J. - \ 2017
Trends in Plant Science 22 (2017)4. - ISSN 1360-1385 - p. 338 - 350.
A striking feature of the angiosperms that use animals as pollen carriers to sexually reproduce is the great diversity of their flowers with regard to morphology and traits such as color, odor, and nectar. These traits are underpinned by the synthesis of secondary metabolites such as pigments and volatiles, as well as carbohydrates and amino acids, which are used by plants to lure and reward animal pollinators. We review here the knowledge of the metabolic network that supports the biosynthesis of these compounds and the behavioral responses that these molecules elicit in the animal pollinators. Such knowledge provides us with a deeper insight into the ecology and evolution of plant-pollinator interactions, and should help us to better manage these ecologically essential interactions in agricultural ecosystems. Novel routes for the biosynthesis of floral volatiles in unusual subcellular compartments are being identified and new theories on the emission of scent are proposed.Key genes in betalain biosynthesis have been identified and new theories on the evolutionary origin of the pathway have been suggested.Master regulators that coordinately control the production of pigments and scent in flowers are emerging.Loci have been identified that contribute to reproductive isolation by pollination preferences for visual and olfactory cues and ultimately lead to speciation.
Combined Use of Genome-Wide Association Data and Correlation Networks Unravels Key Regulators of Primary Metabolism in Arabidopsis thaliana
Wu, Si ; Alseekh, Saleh ; Cuadros-Inostroza, Álvaro ; Fusari, Corina M. ; Mutwil, Marek ; Kooke, Rik ; Keurentjes, Joost B. ; Fernie, Alisdair R. ; Willmitzer, Lothar ; Brotman, Yariv - \ 2016
Plos Genetics 12 (2016)10. - ISSN 1553-7390

Plant primary metabolism is a highly coordinated, central, and complex network of biochemical processes regulated at both the genetic and post-translational levels. The genetic basis of this network can be explored by analyzing the metabolic composition of genetically diverse genotypes in a given plant species. Here, we report an integrative strategy combining quantitative genetic mapping and metabolite‒transcript correlation networks to identify functional associations between genes and primary metabolites in Arabidopsis thaliana. Genome-wide association study (GWAS) was used to identify metabolic quantitative trait loci (mQTL). Correlation networks built using metabolite and transcript data derived from a previously published time-course stress study yielded metabolite‒transcript correlations identified by covariation. Finally, results obtained in this study were compared with mQTL previously described. We applied a statistical framework to test and compare the performance of different single methods (network approach and quantitative genetics methods, representing the two orthogonal approaches combined in our strategy) with that of the combined strategy. We show that the combined strategy has improved performance manifested by increased sensitivity and accuracy. This combined strategy allowed the identification of 92 candidate associations between structural genes and primary metabolites, which not only included previously well-characterized gene‒metabolite associations, but also revealed novel associations. Using loss-of-function mutants, we validated two of the novel associations with genes involved in tyrosine degradation and in β-alanine metabolism. In conclusion, we demonstrate that applying our integrative strategy to the largely untapped resource of metabolite–transcript associations can facilitate the discovery of novel metabolite-related genes. This integrative strategy is not limited to A. thaliana, but generally applicable to other plant species.

Allelic differences in a vacuolar invertase affect Arabidopsis growth at early plant development
Coluccio Leskow, Carla ; Kamenetzky, Laura ; Dominguez, Pia Guadalupe ; Díaz Zirpolo, José Antonio ; Obata, Toshihiro ; Costa, Hernán ; Martí, Marcelo ; Taboga, Oscar ; Keurentjes, Joost ; Sulpice, Ronan ; Ishihara, Hirofumi ; Stitt, Mark ; Fernie, Alisdair Robert ; Carrari, Fernando - \ 2016
Journal of Experimental Botany 67 (2016)14. - ISSN 0022-0957 - p. 4091 - 4103.
Arabidopsis - Biomass - Inhibitor - Near isogenic line - Quantitative trait loci - Vacuolar invertase

Improving carbon fixation in order to enhance crop yield is a major goal in plant sciences. By quantitative trait locus (QTL) mapping, it has been demonstrated that a vacuolar invertase (vac-Inv) plays a key role in determining the radical length in Arabidopsis. In this model, variation in vac-Inv activity was detected in a near isogenic line (NIL) population derived from a cross between two divergent accessions: Landsberg erecta (Ler) and Cape Verde Island (CVI), with the CVI allele conferring both higher Inv activity and longer radicles. The aim of the current work is to understand the mechanism(s) underlying this QTL by analyzing structural and functional differences of vac-Inv from both accessions. Relative transcript abundance analyzed by quantitative real-time PCR (qRT-PCR) showed similar expression patterns in both accessions; however, DNA sequence analyses revealed several polymorphisms that lead to changes in the corresponding protein sequence. Moreover, activity assays revealed higher vac-Inv activity in genotypes carrying the CVI allele than in those carrying the Ler allele. Analyses of purified recombinant proteins showed a similar K m for both alleles and a slightly higher V max for that of Ler. Treatment of plant extracts with foaming to release possible interacting Inv inhibitory protein(s) led to a large increase in activity for the Ler allele, but no changes for genotypes carrying the CVI allele. qRT-PCR analyses of two vac-Inv inhibitors in seedlings from parental and NIL genotypes revealed different expression patterns. Taken together, these results demonstrate that the vac-Inv QTL affects root biomass accumulation and also carbon partitioning through a differential regulation of vac-Inv inhibitors at the mRNA level.

JUNGBRUNNEN1, a Reactive Oxygen Species–Responsive NAC Transcription Factor, Regulates Longevity in Arabidopsis
Wu, A. ; Devi Allu, A. ; Garapati, P. ; Siddiqui, H. ; Dortay, H. ; Zanor, M.I. ; Amparo Asensi-Fabado, M. ; Munne´ -Bosch, S. ; Antonio, C. ; Tohge, T. ; Fernie, A.R. ; Kaufmann, K. ; Xue, G.P. ; Mueller-Roeber, B. ; Balazadeh, S. - \ 2012
The Plant Cell 24 (2012)2. - ISSN 1040-4651 - p. 482 - 506.
programmed cell-death - heat-stress response - leaf senescence - gene-expression - hydrogen-peroxide - oxidative stress - glucosinolate biosynthesis - comprehensive analysis - environmental-stress - functional-genomics
The transition from juvenility through maturation to senescence is a complex process that involves the regulation of longevity. Here, we identify JUNGBRUNNEN1 (JUB1), a hydrogen peroxide (H2O2)-induced NAC transcription factor, as a central longevity regulator in Arabidopsis thaliana. JUB1 overexpression strongly delays senescence, dampens intracellular H2O2 levels, and enhances tolerance to various abiotic stresses, whereas in jub1-1 knockdown plants, precocious senescence and lowered abiotic stress tolerance are observed. A JUB1 binding site containing a RRYGCCGT core sequence is present in the promoter of DREB2A, which plays an important role in abiotic stress responses. JUB1 transactivates DREB2A expression in mesophyll cell protoplasts and transgenic plants and binds directly to the DREB2A promoter. Transcriptome profiling of JUB1 overexpressors revealed elevated expression of several reactive oxygen species–responsive genes, including heat shock protein and glutathione S-transferase genes, whose expression is further induced by H2O2 treatment. Metabolite profiling identified elevated Pro and trehalose levels in JUB1 overexpressors, in accordance with their enhanced abiotic stress tolerance. We suggest that JUB1 constitutes a central regulator of a finely tuned control system that modulates cellular H2O2 level and primes the plants for upcoming stress through a gene regulatory network that involves DREB2A
Inhibition of aconitase in citrus fruit callus results in a metabolic shift towards amino acid biosynthesis
Degu, A. ; Hatew, B. ; Nunes-Nesi, A. ; Shlizerman, L. ; Zur, N. ; Fernie, A.R. ; Blumwald, E. ; Sadka, A. - \ 2011
Planta 234 (2011)3. - ISSN 0032-0935 - p. 501 - 513.
iron-regulatory protein-1 - succinic-semialdehyde dehydrogenase - rat liver mitochondrial - rna-binding activity - gene-expression - acetohydroxyacid synthase - isocitrate dehydrogenase - alanine aminotransferase - competitive inhibitor - glyoxylate reductase
Citrate, a major determinant of citrus fruit quality, accumulates early in fruit development and declines towards maturation. The isomerization of citrate to isocitrate, catalyzed by aconitase is a key step in acid metabolism. Inhibition of mitochondrial aconitase activity early in fruit development contributes to acid accumulation, whereas increased cytosolic activity of aconitase causes citrate decline. It was previously hypothesized that the block in mitochondrial aconitase activity, inducing acid accumulation, is caused by citramalate. Here, we investigated the effect of citramalate and of another aconitase inhibitor, oxalomalate, on aconitase activity and regulation in callus originated from juice sacs. These compounds significantly increased citrate content and reduced the enzyme’s activity, while slightly inducing its protein level. Citramalate inhibited the mitochondrial, but not cytosolic form of the enzyme. Its external application to mandarin fruits resulted in inhibition of aconitase activity, with a transient increase in fruit acidity detected a few weeks later. The endogenous level of citramalate was analyzed in five citrus varieties: its pattern of accumulation challenged the notion of its action as an endogenous inhibitor of mitochondrial aconitase. Metabolite profiling of oxalomalate-treated cells showed significant increases in a few amino acids and organic acids. The activities of alanine transaminase, aspartate transaminase and aspartate kinase, as well as these of two ¿-aminobutyrate (GABA)-shunt enzymes, succinic semialdehyde reductase (SSAR) and succinic semialdehyde dehydrogenase (SSAD) were significantly induced in oxalomalate-treated cells. It is suggested that the increase in citrate, caused by aconitase inhibition, induces amino acid synthesis and the GABA shunt, in accordance with the suggested fate of citrate during the acid decline stage in citrus fruit.
Genetics, Genomics and Metabolomics
Fernie, A.R. ; Keurentjes, J.J.B. - \ 2011
In: Annual Plant Reviews / Hall, R., Blackwell Publishing Ltd. (Annual Plant Reviews 43) - p. 219 - 259.
Metabolomics approaches enable the parallel assessment of the levels of a broad range of metabolites. They have been documented to have great value in phenotyping and diagnostic analyses in plants as well as showing great promise as a tool for bio-prospecting novel pharmaceuticals. These tools have recently been turned to evaluation of the natural variance apparent in metabolite composition both in the model species Arabidopsis thaliana and a range of crop species. Here, we describe exciting progress made in the identification of the genetic determinants of plant chemical composition, focusing on the application of various different metabolomics strategies. We focus on the integration of these data with those other high-throughput technologies and discuss the value of such approaches for gaining fundamental insights into metabolic and even cellular regulation. Finally, we discuss the fact that when considered from an applied perspective metabolomics represents an important addition to the tools currently employed in genomicsassisted selection for crop improvement
Identification of Genes in the Phenylalanine Metabolic Pathway by Ectopic Expression of a MYB Transcription Factor in Tomato Fruit
Cin, V. Dal; Tieman, D.M. ; Tohge, T. ; McQuinn, R. ; Vos, C.H.R. de; Osorio, S. ; Schmelz, E.A. ; Taylor, M.G. ; Smits-Kroon, M.T. ; Schuurink, R.C. ; Haring, M.A. ; Giovannoni, J. ; Fernie, A.R. ; Klee, H.J. - \ 2011
The Plant Cell 23 (2011)7. - ISSN 1040-4651 - p. 2738 - 2753.
chromatography-mass spectrometry - prephenate aminotransferase - amino-acids - lycopersicon-esculentum - arabidopsis-thaliana - escherichia-coli - microarray data - cell-cultures - biosynthesis - arogenate
Altering expression of transcription factors can be an effective means to coordinately modulate entire metabolic pathways in plants. It can also provide useful information concerning the identities of genes that constitute metabolic networks. Here, we used ectopic expression of a MYB transcription factor, Petunia hybrida ODORANT1, to alter Phe and phenylpropanoid metabolism in tomato (Solanum lycopersicum) fruits. Despite the importance of Phe and phenylpropanoids to plant and human health, the pathway for Phe synthesis has not been unambiguously determined. Microarray analysis of ripening fruits from transgenic and control plants permitted identification of a suite of coregulated genes involved in synthesis and further metabolism of Phe. The pattern of coregulated gene expression facilitated discovery of the tomato gene encoding prephenate aminotransferase, which converts prephenate to arogenate. The expression and biochemical data establish an arogenate pathway for Phe synthesis in tomato fruits. Metabolic profiling and 13C flux analysis of ripe fruits further revealed large increases in the levels of a specific subset of phenylpropanoid compounds. However, while increased levels of these human nutrition-related phenylpropanoids may be desirable, there were no increases in levels of Phe-derived flavor volatiles.
Transcriptome and Metabolite Profiling Show That APETALA2a Is a Major Regulator of Tomato Fruit Ripening
Karlova, R.B. ; Rosin, F.M.A. ; Busscher-Lange, J. ; Parapunova, V.A. ; Do, P.T. ; Fernie, A.R. ; Fraser, P.D. ; Baxter, C. ; Angenent, G.C. ; Maagd, R.A. de - \ 2011
The Plant Cell 23 (2011)3. - ISSN 1040-4651 - p. 923 - 941.
homeotic gene apetala2 - ethylene biosynthesis - flower development - 1-aminocyclopropane-1-carboxylate synthase - chromoplast differentiation - lycopersicon-esculentum - expression analysis - arabidopsis flower - seed development - organ identity
Fruit ripening in tomato (Solanum lycopersicum) requires the coordination of both developmental cues as well as the plant hormone ethylene. Although the role of ethylene in mediating climacteric ripening has been established, knowledge regarding the developmental regulators that modulate the involvement of ethylene in tomato fruit ripening is still lacking. Here, we show that the tomato APETALA2a (AP2a) transcription factor regulates fruit ripening via regulation of ethylene biosynthesis and signaling. RNA interference (RNAi)-mediated repression of AP2a resulted in alterations in fruit shape, orange ripe fruits, and altered carotenoid accumulation. Microarray expression analyses of the ripe AP2 RNAi fruits showed altered expression of genes involved in various metabolic pathways, such as the phenylpropanoid and carotenoid pathways, as well as in hormone synthesis and perception. Genes involved in chromoplast differentiation and other ripening-associated processes were also differentially expressed, but softening and ethylene biosynthesis occurred in the transgenic plants. Ripening regulators RIPENING-INHIBITOR, NON-RIPENING, and COLORLESS NON-RIPENING (CNR) function upstream of AP2a and positively regulate its expression. In the pericarp of AP2 RNAi fruits, mRNA levels of CNR were elevated, indicating that AP2a and CNR are part of a negative feedback loop in the regulation of ripening. Moreover, we demonstrated that CNR binds to the promoter of AP2a in vitro
SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato.
Vogel, J.T. ; Walter, M.H. ; Giavalisco, P. ; Lytovchenko, A. ; Kohlen, W. ; Charnikhova, T. ; Simkin, A.J. ; Goulet, C. ; Strack, D. ; Bouwmeester, H.J. ; Fernie, A.R. ; Klee, H.J. - \ 2010
The Plant Journal 61 (2010)2. - ISSN 0960-7412 - p. 300 - 311.
carotenoid cleavage dioxygenase - root-derived signal - striga-lutea lour - germination stimulants - liquid-chromatography - plant architecture - yellow pigment - orobanche spp. - arabidopsis - genes
The regulation of shoot branching is an essential determinant of plant architecture, integrating multiple external and internal signals. One of the signaling pathways regulating branching involves the MAX (more axillary branches) genes. Two of the genes within this pathway, MAX3/CCD7 and MAX4/CCD8, encode carotenoid cleavage enzymes involved in generating a branch-inhibiting hormone, recently identified as strigolactone. Here, we report the cloning of SlCCD7 from tomato. As in other species, SlCCD7 encodes an enzyme capable of cleaving cyclic and acyclic carotenoids. However, the SlCCD7 protein has 30 additional amino acids of unknown function at its C terminus. Tomato plants expressing a SlCCD7 antisense construct display greatly increased branching. To reveal the underlying changes of this strong physiological phenotype, a metabolomic screen was conducted. With the exception of a reduction of stem amino acid content in the transgenic lines, no major changes were observed. In contrast, targeted analysis of the same plants revealed significantly decreased levels of strigolactone. There were no significant changes in root carotenoids, indicating that relatively little substrate is required to produce the bioactive strigolactones. The germination rate of Orobanche ramosa seeds was reduced by up to 90% on application of extract from the SlCCD7 antisense lines, compared with the wild type. Additionally, upon mycorrhizal colonization, C13 cyclohexenone and C14 mycorradicin apocarotenoid levels were greatly reduced in the roots of the antisense lines, implicating SlCCD7 in their biosynthesis. This work demonstrates the diverse roles of MAX3/CCD7 in strigolactone production, shoot branching, source–sink interactions and production of arbuscular mycorrhiza-induced apocarotenoids.
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