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Publications

Walter, M. H.; Stauder, R.; Tissier, A. Evolution of root-specific carotenoid precursor pathways for apocarotenoid signal biogenesis Plant Sci 233, 1-10, (2015) DOI: 10.1016/j.plantsci.2014.12.017

Various cleavage products of C40 carotenoid substrates are formed preferentially or exclusively in roots. Such apocarotenoid signaling or regulatory compounds differentially induced in roots during environmental stress responses including root colonization by arbuscular mycorrhizal fungi include ABA, strigolactones and C13 α-ionol/C14 mycorradicin derivatives. The low carotenoid levels in roots raise the question of whether there is a regulated precursor supply channeled into apocarotenoid formation distinct from default carotenoid pathways. This review describes root-specific isogene components of carotenoid pathways toward apocarotenoid formation, highlighting a new PSY3 class of phytoene synthase genes in dicots. It is clearly distinct from the monocot PSY3 class co-regulated with ABA formation. At least two members of the exclusive dicot PSY3s are regulated by nutrient stress and mycorrhization. This newly recognized dicot PSY3 (dPSY3 vs. mPSY3 from monocots) class probably represents an ancestral branch in the evolution of the plant phytoene synthase family. The evolutionary history of PSY genes is compared with the evolution of MEP pathway isogenes encoding 1-deoxy-d-xylulose 5-phosphate synthases (DXS), particularly DXS2, which is co-regulated with dPSY3s in mycorrhizal roots. Such stress-inducible isoforms for rate-limiting steps in root carotenogenesis might be components of multi-enzyme complexes committed to apocarotenoid rather than to carotenoid formation.
Publications

López-Ráez, J. A.; Fernández, I.; García, J. M.; Berrio, E.; Bonfante, P.; Walter, M. H.; Pozo, M. J. Differential spatio-temporal expression of carotenoid cleavage dioxygenases regulates apocarotenoid fluxes during AM symbiosis Plant Sci 230 , 59-69, (2014) DOI: 10.1016/j.plantsci.2014.10.010

Apocarotenoids are a class of compounds that play important roles in nature. In recent years, a prominent role for these compounds in arbuscular mycorrhizal (AM) symbiosis has been shown. They are derived from carotenoids by the action of the carotenoid cleavage dioxygenase (CCD) enzyme family. In the present study, using tomato as a model, the spatio-temporal expression pattern of the CCD genes during AM symbiosis establishment and functioning was investigated. In addition, the levels of the apocarotenoids strigolactones (SLs), C13 α-ionol and C14 mycorradicin (C13/C14) derivatives were analyzed. The results suggest an increase in SLs promoted by the presence of the AM fungus at the early stages of the interaction, which correlated with an induction of the SL biosynthesis gene SlCCD7. At later stages, induction of SlCCD7 and SlCCD1 expression in arbusculated cells promoted the production of C13/C14 apocarotenoid derivatives. We show here that the biosynthesis of apocarotenoids during AM symbiosis is finely regulated throughout the entire process at the gene expression level, and that CCD7 constitutes a key player in this regulation. Once the symbiosis is established, apocarotenoid flux would be turned towards the production of C13/C14 derivatives, thus reducing SL biosynthesis and maintaining a functional symbiosis.
Books and chapters

Walter, M. H.  Role of carotenoid metabolism in the Arbuscular Mycorrhizal symbiosis. ( F. de Bruijn). 513-524, (2013) ISBN: 9781118297674 DOI: 10.1002/9781118297674.ch48

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Books and chapters

Walter, M.H., Floss, D.S., Paetzold, H., Manke, K., Vollrath, J., Brandt, W. & Strack, D. Control of plastidial isoprenoid precursor supply: Divergent 1-deoxy-d-xylulose 5-phosphate synthase (DXS) isogenes regulate the allocation to primary and secondary metabolism (T.J. Bach, M. Rohmer eds.). 251-270, (2013) ISBN: 978-1-4614-4062-8 DOI: 10.1007/978-1-4614-4063-5

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Publications

Walter, M. H.; Strack, D. Carotenoids and their cleavage products: Biosynthesis and functions Nat Prod Rep 28, 663-692, (2011) DOI: 10.1039/C0NP00036A

Covering: up to mid-2010This review focuses on plant carotenoids, but it also includes progress made on microbial and animal carotenoid metabolism to better understand the functions and the evolution of these structurally diverse compounds with a common backbone. Plants have evolved isogenes for specific key steps of carotenoid biosynthesis with differential expression profiles, whose characteristic features will be compared. Perhaps the most exciting progress has been made in studies of carotenoid cleavage products (apocarotenoids) with an ever-expanding variety of novel functions being discovered. This review therefore covers structural, molecular genetic and functional aspects of carotenoids and apocarotenoids alike. Apocarotenoids are specifically tailored from carotenoids by a family of oxidative cleavage enzymes, but whether there are contributions to their generation from chemical oxidation, photooxidation or other mechanisms is largely unknown. Control of carotenoid homeostasis is discussed in the context of biosynthetic and degradative reactions but also in the context of subcellular environments for deposition and sequestration within and outside of plastids. Other aspects of carotenoid research, including metabolic engineering and synthetic biology approaches, will only be covered briefly.
Publications

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. SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato Plant J 61, 300-311 , (2010) DOI: 10.1111/j.1365-313X.2009.04056.x

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.
Publications

Walter, M. H.; Floss, D. S.; Strack, D. Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232, 1-17, (2010) DOI: 10.1007/s00425-010-1156-3

Apocarotenoids are tailored from carotenoids by oxidative enzymes [carotenoid cleavage oxygenases (CCOs)], cleaving specific double bonds of the polyene chain. The cleavage products can act as hormones, signaling compounds, chromophores and scent/aroma constituents. Recent advances were the identification of strigolactones as apocarotenoids and the description of their novel role as shoot branching inhibitor hormones. Strigolactones are also involved in plant signaling to both harmful (parasitic weeds) and beneficial [arbuscular mycorrhizal (AM) fungi] rhizosphere residents. This review describes the progress in the characterization of CCOs, termed CCDs and NCEDs, in plants. It highlights the importance of sequential cleavage reactions of C40 carotenoid precursors, the apocarotenoid cleavage oxygenase (ACO) nature of several CCOs and the topic of compartmentation. Work on the biosynthesis of abundant C13 cyclohexenone and C14 mycorradicin apocarotenoids in mycorrhizal roots has revealed a new role of CCD1 as an ACO of C27 apocarotenoid intermediates, following their predicted export from plastid to cytosol. Manipulation of the AM-induced apocarotenoid pathway further suggests novel roles of C13 apocarotenoids in controlling arbuscule turnover in the AM symbiosis. CCD7 has been established as a biosynthetic crosspoint, controlling both strigolactone and AM-induced C13 apocarotenoid biosynthesis. Interdependence of the two apocarotenoid pathways may thus play a role in AM-mediated reduction of parasitic weed infestations. Potential scenarios of C13 scent/aroma volatile biogenesis are discussed, including the novel mechanism revealed from mycorrhizal roots. The recent progress in apocarotenoid research opens up new perspectives for fundamental work, but has also great application potential for the horticulture, food and fragrance industries.
Publications

Paetzold, H.; Garms, S.; Bartram, S.; Wieczorek, J.; Urós-Gracia, E.-M.; Rodríguez-Concepción, M.; Boland, W.; Strack, D.; Hause, B.; Walter, M. H. The Isogene 1-Deoxy-D-Xylulose 5-Phosphate Synthase 2 Controls Isoprenoid Profiles, Precursor Pathway Allocation, and Density of Tomato Trichomes Mol Plant 3, 904-916 , (2010) DOI: 10.1093/mp/ssq032

Plant isoprenoids are formed from precursors synthesized by the mevalonate (MVA) pathway in the cytosol or by the methyl-D-erythritol 4-phosphate (MEP) pathway in plastids. Although some exchange of precursors occurs, cytosolic sesquiterpenes are assumed to derive mainly from MVA, while plastidial monoterpenes are produced preferentially from MEP precursors. Additional complexity arises in the first step of the MEP pathway, which is typically catalyzed by two divergent 1-deoxy-D-xylulose 5-phosphate synthase isoforms (DXS1, DXS2). In tomato (Solanum lycopersicum), the SlDXS1 gene is ubiquitously expressed with highest levels during fruit ripening, whereas SlDXS2 transcripts are abundant in only few tissues, including young leaves, petals, and isolated trichomes. Specific down-regulation of SlDXS2 expression was performed by RNA interference in transgenic plants to investigate feedback mechanisms. SlDXS2 down-regulation led to a decrease in the monoterpene β-phellandrene and an increase in two sesquiterpenes in trichomes. Moreover, incorporation of MVA-derived precursors into residual monoterpenes and into sesquiterpenes was elevated as determined by comparison of 13C to 12C natural isotope ratios. A compensatory up-regulation of SlDXS1 was not observed. Down-regulated lines also exhibited increased trichome density and showed less damage by leaf-feeding Spodoptera littoralis caterpillars. The results reveal novel, non-redundant roles of DXS2 in modulating isoprenoid metabolism and a pronounced plasticity in isoprenoid precursor allocation.
Publications

Floss, D. S.; Walter, M. H. Role of carotenoid cleavage dioxygenase 1 (CCD1) in apocarotenoid biogenesis revisited Plant Signal Behav 4, 172-175, (2009) DOI: 10.4161/psb.4.3.7840

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Publications

Walter, M. H.; Floß, D. S.; Strack, D. Die facettenreiche Welt der Apocarotinoide. Farben, Düfte, Aromen und Hormone Biologie in unserer Zeit 39, 336-344, (2009) DOI: 10.1002/biuz.200910402

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