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Metabolomics Analysis Reveals Tissue-Specific Metabolite International Journal of Molecular Sciences Article Metabolomics Analysis Reveals Tissue-Specific Metabolite Compositions in Leaf Blade and Traps of Carnivorous Nepenthes Plants 1,2, 3, 3 Alberto Dávila-Lara y , Carlos E. Rodríguez-López y , Sarah E. O’Connor and Axel Mithöfer 1,* 1 Research Group Plant Defense Physiology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; [email protected] 2 Departamento de Biología, Universidad Nacional Autónoma de Nicaragua-León (UNAN), 21000 León, Nicaragua 3 Department of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; [email protected] (C.E.R.-L.); [email protected] (S.E.O.) * Correspondence: [email protected] These authors contributed equally to this work. y Received: 18 May 2020; Accepted: 17 June 2020; Published: 19 June 2020 Abstract: Nepenthes is a genus of carnivorous plants that evolved a pitfall trap, the pitcher, to catch and digest insect prey to obtain additional nutrients. Each pitcher is part of the whole leaf, together with a leaf blade. These two completely different parts of the same organ were studied separately in a non-targeted metabolomics approach in Nepenthes x ventrata, a robust natural hybrid. The first aim was the analysis and profiling of small (50–1000 m/z) polar and non-polar molecules to find a characteristic metabolite pattern for the particular tissues. Second, the impact of insect feeding on the metabolome of the pitcher and leaf blade was studied. Using UPLC-ESI-qTOF and cheminformatics, about 2000 features (MS/MS events) were detected in the two tissues. They showed a huge chemical diversity, harboring classes of chemical substances that significantly discriminate these tissues. Among the common constituents of N. x ventrata are phenolics, flavonoids and naphthoquinones, namely plumbagin, a characteristic compound for carnivorous Nepenthales, and many yet-unknown compounds. Upon insect feeding, only in pitchers in the polar compounds fraction, small but significant differences could be detected. By further integrating information with cheminformatics approaches, we provide and discuss evidence that the metabolite composition of the tissues can point to their function. Keywords: Nepenthes; carnivorousplants; UPLC-qToF-MS;metabolomics; tissuespecificity;cheminformatics 1. Introduction Metamorphosis of plant organs is a common feature in higher plants and often an adaptation to the particular environment. Metamorphosis covers genetically fixed changes in both morphology and anatomy leading to new structural or functional modifications. In higher plants, leaves are mainly involved in photosynthesis and transpiration, but many leaf metamorphoses are also known for exhibiting new functions. Examples are spines as protection against herbivores (cacti), needles to reduce water loss (conifers), bulbs for storage of water and nutrients (onion), and tendrils for climbing (pea). Striking structures of leaf metamorphosis are found in many carnivorous plants that live on nutrient-poor soil and catch animal prey to get additional nutrients, such as nitrogen and phosphate [1,2]. Here, the leaves are employed in catching prey, mainly insects. For instance, in Venus flytrap (Dionaea muscipula), rapidly closing snap traps are found, in sundew (Drosera) species sticky Int. J. Mol. Sci. 2020, 21, 4376; doi:10.3390/ijms21124376 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 2 of 18 Int. J. Mol. Sci. 2020, 21, 4376 2 of 17 Int. J. Mol. Sci. 2019, 20, x FOR PEER REVIEW 2 of 18 sticky flypaper traps, and in bladderwort (Utricularia) species sucking bladder traps [1,2]. Another typestickyflypaper of flypaper trap traps, is realized andtraps in, andbladderwort in so in-called bladderwort pitcher (Utricularia) (trapsUtricularia speciesthat can) species sucking be found sucking bladder in the bladder trapsgenus [ 1 Nepenthes,traps2]. Another [1,2 ](Figure. Another type 1) of, occurringtypetrap isof realized trap in isSoutheast realized in so-called Asiain so pitcher.- called traps pitcher that traps can bethat found can be in thefound genus in theNepenthes genus Nepenthes(Figure1), (Figure occurring 1), occurringin Southeast in Southeast Asia. Asia. Figure 1. Nepenthes x ventrata. Natural hybrid of N. ventricosa and N. alata. Figure 1. Nepenthes x ventrata . Natural Natural hybrid hybrid of of N. ventricosa and N. alata .. These passive traps attract prey to the pitcher opening, the peristome, which is extremely slippery forThese insectsThese passive causing passive traps trapsthem attract attract to preyfall prey into to the tothe thepitcher pitcher. pitcher opening, The opening, lower the the partperistome, peristome, of the pitcherwhich which isis extremely extremelyfilled with slippery a fluid wherefor insects the preycausing drowns. them Subsequently, to fall into the plant pitcher.-derived The The lowerhydrolytic lower part part enzymesof of the pitcher inside is the filled filled fluid with digest a fluidfluid the preywhere and the generate prey drowns. absorbab Subsequently, le forms of plant-derivedplant nutrients-derived, which hydrolytic are taken enzymes up and inside delivered the fluid fluid further digest to the plantprey andandbody generategenerate through absorbable absorbab bi-functionalle forms forms glands of of nutrients, nutrients [2,3]. whichIn, whichNepenthes are are taken speciestaken up andup, the and delivered whole delivered leaf further underwentfurther to the to plant thean extensiveplantbody throughbody metamorphosis: through bi-functional bi-functional the glands typical glands [2,3 ].leaf In [2,3] Nepentheslamina. In Nepenthes(synospecies,nym: thespecies leaf whole blade), the leaf wholeturned underwent leaf into underwent a an pit extensivecher foran catchingextensivemetamorphosis: prey, metamorphosis: the the petiole typical intothe leaf typicala lamina tendril leaf (synonym: to lamina climb, leaf(synoand blade) thenym: leaf turnedleaf base blade)into into a turneda pitcher basal in forleafto catching-aderived pitcher prey, leaffor bladecatchingthe petiole (from prey, into now the a on: tendril petiole leaf toblade) climb,into substitutinga andtendril the to leaf theclimb, base lamina intoand toathe basal ensure leaf leaf-derived basephotosynthesis into a leaf basal blade (Figure leaf (from-derived 2) [4,5] now . leaf on: bladeleaf blade) (from substituting now on: leaf the blade) lamina substituting to ensure photosynthesisthe lamina to ensure (Figure photosynthesis2)[4,5]. (Figure 2) [4,5]. (A) (B) Lamina (A) (B) Lamina Petiole Petiole Leaf base Leaf base Stem Stem Tendril Lamina Tendril LaminaPitcher Pitcher Figure 2.2. ComparisonComparison of of leaf leaf morphology. morphology. (A )(NepenthesA) Nepenthes x ventrata x ventrataleaf. (leaf.B) Typical (B) Typical foliage leavesfoliage (upper), leaves Nepenthes leaf (below). In italics, the leaf parts developed in Nepenthes as result of metamorphosis (upper),Figure 2. NepenthesComparison leaf of (below). leaf morphology. In italics , (Athe) Nepenthes leaf parts x ventratadeveloped leaf. in(B )Nepenthes Typical foliageas result leaves of of the typical leaf parts. For further explanation, see the text. Copyright © of drawing (B) held by metamorphosis(upper), Nepenthes of theleaf typical(below). leaf In parts. italics For, the further leaf partsexplanation developed, see inthe Nepenthes text. Copyright as result © of Sarah Zunk. drawingmetamorphosis (B) held of by the Sarah typical Zunk. leaf parts. For further explanation, see the text. Copyright © of drawingFor many (B years,) held by scientists Sarah Zunk. studied the different trapping mechanisms in order to understand their function and biomechanics. However, changes and adaptations in leaf morphology and anatomy also come along with changes in the physiology, biochemistry, and molecular biology of carnivorous plants. Thus, in recent years, many studies in carnivorous plants focused more and more on molecular aspects 2 2 Int. J. Mol. Sci. 2020, 21, 4376 3 of 17 and “omics” approaches, except metabolomics. Those studies have produced more and deeper insights in the molecular events accompanying the various steps necessary for successful prey hunting and digestion, suggesting, for example, that plant carnivory originates from defense mechanisms [6–12]; however, most studies are still related to the particular traps. In Nepenthes, the pitcher fluid was investigated in detail, including its proteome [13–15] and the composition of organic and inorganic low-molecular-weight compounds [16]. Based on such studies, we learned that the pitcher fluids consist of enzymes necessary for digestion and also defensive proteins belonging to the group of pathogenesis-related proteins [17]. Moreover, the pitcher fluid is poor in inorganic nutrients and contains secondary metabolites with antimicrobial properties, i.e., naphthoquinones; droserone and 5-O-methyl droserone are described for N. khasiana [18] and plumbagin and 7-methyl-juglon for N. ventricosa [16]. These compounds are not widespread in plants but very often occur in carnivorous plants of the order Nepenthales [19], a sensu stricto sister group to Caryophyllales [5]. For Nepenthes, some of these naphthoquinones were described as inducible by chitin and prey [18,20], suggesting a functional role after prey catch. Naphthoquinones are highly bioactive compounds with defense-related properties [21]. Therefore, it has for a long time been suggested that these compounds are involved in protection against various microbes and
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