Plants produce tens of thousands of molecules called secondary metabolites that are thought to help them cope with threats from their environment, such as attack by insects or ultraviolet radiation from the sun. Wild coyote tobacco plants produce large amounts of a particular class of secondary metabolite known as DTGs. Insects feeding on tobacco plants containing DTGs cause less damage and produce fewer offspring

Plants modify many secondary metabolites by attaching tags known as malonyl groups to them. Enzymes called malonyl transferases take a malonyl group from another substrate and attach it to the secondary metabolite. This process can be repeated so that an individual secondary metabolite molecule may have many malonyl groups attached to it. Previous studies have shown that insects feeding on tobacco plants trigger more malonyl groups to be attached to DTGs, but it is not clear what effect this has on the plants.

To simulate attack by an insect, Li et al. punctured holes in the leaves of tobacco plants and applied saliva from tobacco hornworms. The experiments show that more DTGs modified with malonyl groups accumulated in these plants compared to untreated plants. However, there was no change in the average number of malonyl groups added to individual DTGs during the modification process. Further experiments show that a malonyl transferase enzyme called NaMaT1 adds malonyl groups to DTGs in coyote tobacco plants. The flowers of plants that produce less of this protein have shorter styles (a tube structure that guides pollen to the egg cells at the base of the flower) and are less fertile than flowers in normal plants.

These experiments demonstrate that, along with helping plants to defend themselves from herbivores, DTGs regulate how flowers grow and develop. It was generally thought that secondary metabolites do not play important roles in how plants grow when they are not under stress. Indeed, plant breeders frequently select crops that produce lower levels of secondary metabolites in order to increase their nutritional value. Therefore, the findings of Li et al. may help improve the outcomes of crop breeding programs.

Malonylation is a ubiquitous modification of proteins and specialized metabolites. In plant specialized metabolism, the malonyl group is largely transferred from malonyl-coenzyme A (Malonyl-CoA) to the C’6 of the glycosyl moiety of glucoconjugates (Taguchi et al., 2005). The malonyl residue is thought to confer structural diversity, stability, and solubility to the decorated metabolites and provide a means of detoxifying xenobiotics (Suzuki et al., 2002; Taguchi et al., 2005; Koirala et al., 2014; Suzuki et al., 2004). Malonylation of anthocyanins enhances pigment stability and color intensity at the pH of the intracellular milieus (Suzuki et al., 2002). In addition, malonylated anthocyanins are preferentially transported to vacuoles in Arabidopsis thaliana (Zhao et al., 2011). The malonylation of glycosides is catalyzed by malonyltransferases, members of the biochemically versatile BAHD acyltransferase family (D'Auria, 2006). Although tens of malonyltransferases have been identified and functionally characterized in vitro (Luo et al., 2007; Manjasetty et al., 2012; Bontpart et al., 2015), their in vivo functions are largely unknown.

17-hydroxygeranyllinalool diterpene glycosides (DTGs) are abundant (mg/g FW) secondary metabolites in green tissues of many solanaceous plants, including tobacco (Nicotiana spp.), pepper (Capsicum annuum) and wolfberry (Lycium chinense) (Jassbi et al., 2006; Lee et al., 2008; Heiling et al., 2010). DTGs consist of a 17-hydroxygeranyllinalool aglycone that is decorated at the C3 and C17 hydroxyl positions by glucose, which in turn is modified by glucose, rhamnose and malonyl moieties, in various combinations (Figure 1A and Figure 1—figure supplement 1). So far, 46 different DTGs (21 chemical formulas and several structural isomers) have been characterized in Nicotiana attenuata, an ecological model plant with a rich portfolio of specialized metabolites; however, the glycoside Lyciumoside IV and its malonylated products, Nicotianoside I and Nicotianoside II, constitute more than 80% of the DTG pool (Poreddy et al., 2015). In N. attenuata, DTGs function in resistance against the specialist herbivore, tobacco hornworm (Manduca sexta) (Lou and Baldwin, 2003; Jassbi et al., 2008; Heiling et al., 2010). The malonylated DTGs are particularly strongly induced by M. sexta feeding and jasmonate signaling (Heiling et al., 2010). The malonyl moieties of DTGs are lost from the DTGs soon after their ingestion by M. sexta larvae due to the alkaline environment of M. sexta oral secretions and midgut (Poreddy et al., 2015). This observation rules out a central role for malonylation of DTGs in antiherbivore defense, and suggests that other arenas need to be explored for potential functions mediated by this malonylation.

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DTG profiles and malonylation percentages under different treatments and developmental stages.

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Figure 1—source data 2

DTG profiles and malonylation percentages across different tissues.

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Specialized metabolites are primarily thought to function in mediating an organism’s ecological interactions, to help optimize Darwinian fitness. Many are produced in response to particular ecological interactions, such as those that are induced in response to specific attackers. However, many secondary metabolites have effects on growth and development which are more specific than those that might result from resource trade-offs between growth and putative defense metabolites (Züst and Agrawal, 2017). For example, the insect feeding-induced glucosinolate breakdown product, indole-3-carbinol, arrests growth by interacting with the auxin receptor Transport Inhibitor Response (TIR1) as an auxin antagonist (Katz et al., 2015). Arabidopsis glucosinolates are also thought to modulate plant biomass, flowering time and the circadian clock, and inhibit root growth (Kerwin et al., 2011; Jensen et al., 2015; Francisco et al., 2016; Malinovsky et al., 2017). Hyper-accumulation of flavonoids is associated with stunted growth and developmental abnormalities, which are assumed to result from effects on auxin transport (Franke et al., 2002; Bonawitz et al., 2014; Steenackers et al., 2017). With the exception of the glucosinolates and flavonoids, little is known about these potential ‘primary’ roles for other branches of specialized (also known as ‘secondary’) metabolism.

The jasmonate signaling pathway is undoubtedly among the most important in plant defense responses to herbivory, regulating a large portion of herbivory-responsive specialized metabolism, including DTGs in N. attenuata (Kessler et al., 2004; Kallenbach et al., 2012; Li et al., 2017; Li et al., 2018). However, jasmonates also regulate root growth, anther dehiscence, male fertility, fruit ripening and senescence (Staswick et al., 1992; Xie et al., 1998; Wasternack et al., 2013; Stitz et al., 2014). Jasmonate signaling-deficient genotypes of N. attenuata, including RNAi lines targeting ALLENE OXIDE CYCLASE (irAOC) and CORONATINE INSENSITIVE 1 (irCOI1), and ectopic expression of Arabidopsis JASMONIC ACID METHYL TRANSFERASE (JMT) and simultaneous silencing of METHYL JASMONATE ESTERASE (MJE) (JMT/mje) which dramatically decreased JA signaling, are reported to have short styles, resulting in reduced fertility (Stitz et al., 2014). Transgenic N. tabacum plants deficient in COI1 also display short styles (Wang et al., 2014). However, the mechanism of this seemingly Nicotiana genus-specific jasmonate-regulated phenotype is completely obscure.

Auxin plays a pivotal role throughout the entire lifespan of a plant, particularly in determination of floral development. It can influence cell division, cell expansion and cell differentiation, and thereby regulate a wide spectrum of developmental processes (Benjamins and Scheres, 2008). Mutants of AtPIN1, a polar auxin transporter, developed naked, pin-shaped inflorescences and abnormalities in all flower parts, confirming that auxin signaling contributes to flower development (Okada, 1991). Consistent with this, mutants of the auxin biosynthesis genes TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA) and YUCCA display severe defects in floral patterning, and complete sterility (Cheng et al., 2006; Stepanova et al., 2008). Auxin can also regulate gynoecium morphogenesis, including style elongation, through a concentration gradient from the apical to the basal part of the gynoecium (Nemhauser et al., 2000).

In this study, we discovered that the malonylation percentage of DTGs is remarkably uniform across development, treatments, and tissue types, and identified the gene involved in this malonylation. We ask whether this uniformity is essential for plant development. Silencing this gene caused strikingly and specifically short styles, and this phenomenon vanished when silencing this gene in DTG-deficient plants. We analyzed phytohormone levels, enzymatic activity, and effects of exogenous application, and all evidence indicated that the short style phenotype is caused by the influence of DTG malonylation status on IAA biosynthesis. Finally, we illustrate that the Nicotiana genus-specific JA-deficient style phenotype is caused by disturbing DTG malonylation patterns. Our work demonstrates that abnormal JA signaling could dysregulate DTG malonylation patterns, thereby affecting plant style development via auxin signaling.

Specialized, or secondary metabolites are usually thought only to mediate plant responses to specific environmental conditions, and not to be directly involved in plant growth, development and reproduction – the providence of primary metabolism. Here, we report that the decoration of specialized metabolites demonstrated remarkable uniformity across development, tissues, and treatments, and found that one malonyltransferase (MaT) contributes significantly to this process. Silencing this gene disturbed 17-hydroxygeranyllinalool diterpene glycoside (DTG) malonylation patterns, and stunted elongation of flower styles during development and fertility by affecting auxin biosynthesis. Abnormal jasmonate signaling could also disturb DTG malonylation patterns, causing similar stylar developmental defects.

Enzyme assays showed that three MaT proteins, NaMaT1-3, catalyze the first step of DTG malonylation, from Lyciumoside IV to Nicotianoside I, and the second step, from Nicotianoside I to Nicotianoside II, in vitro (Figure 2C). As Lyciumoside IV only has two glucose moieties (Figure 1—figure supplement 1) and the abundances of tri-glucosylated core DTGs are too low to purify from plants, we were unable to test the ability of those NaMaTs to catalyze the third malonylation reaction. However, in vivo silencing of NaMaT1 dramatically decreased dimalonylated and trimalonylated DTGs in inflorescences and styles (Figure 4), which indicates that NaMaT1 might also control the third step of the malonylation reaction in planta. Notably, in vivo silencing of NaMaT1 changed individual DTG abundances in complex ways. For example, although the total abundance of dimalonylated DTGs decreased significantly in NaMaT1-silenced styles, the abundance of one dimalonylated DTG, Nicotianoside X, did not change significantly, whereas the abundance of two dimalonylated compounds, Nicotianoside XII and Nicotianoside VII, increased (Figure 4–Figure supplement 1AFigure 4—figure supplement 1A). Currently, we cannot rule out the possibility that some of these changes are not directly mediated by NaMaT1 catalytic activity, but result from systemic influence, such as substrate limitation. Future work should test NaMaT1 substrate specificity for all DTGs, when technology can support the purification of low-abundance components in sufficient amounts. Based on our current results, we infer that NaMaT1 is a malonyl-CoA:DTG malonyltransferase, which may catalyze three consecutive malonylation steps, as reported for Dm3MaT2, which catalyzes consecutive dimalonyl transfers to anthocyanin (Suzuki et al., 2004). Notably, two characterized MaTs in the Nicotiana genus, NbMaT1 and NtMaT1, accept aromatic glycosides as substrate (Taguchi et al., 2005; Liu et al., 2017). Phylogenic and protein identity analysis showed that NbMaT1 and NtMaT1 share the highest sequence similarity with NaMaT2 and NaMaT3, about 90%, whereas the identity with NaMaT1 is 80% (Figure 2A and Figure 2—figure supplement 1B). Moreover, cross-tissue comprehensive nontargeted metabolomics analyses did not reveal any malonylated flavonoids in N. attenuata (Li et al., 2016), although NaMaT1 is highly expressed in M. sexta-infested leaves. Thus, we assume that NaMaT1 mainly functions in DTG malonylation in planta, and NaMaT2 and NaMaT3 could also accept aromatic glycosides as substrates, like NbMaT1 and NtMaT1.

Specialized metabolites are thought to be strongly regulated by environmental cues, and are often thought to function in a plant’s adaptive responses to environmental changes. Here, our data revealed remarkable uniformity of DTG malonylation status, although individual DTGs are plastic. For the regulation of DTG biosynthesis, feed-back and feed-forward regulation are both described by Heiling et al. (in preparation): silencing a rhamnosyltransferase gene inhibits the transcript accumulation of all upstream genes, and silencing NaGGPPS also suppresses transcript accumulation of downstream biosynthetic genes. Here, we show that VIGS of NaMaT1 tended to increase both NaMaT2 and NaMaT3 expression, and significantly increased NaGLS expression (Figure 3—figure supplement 1B and C). Two or more elements oppositely controlling one process is a powerful homeostatic strategy, as is found in JA-Ile conjugation and JA-Ile hydroxylation which maintains JA-Ile homeostasis (Kang et al., 2006; Woldemariam et al., 2012). Here, the induction of NaMaT1 and suppression of NaMaT2 and NaMaT3 in response to M. sexta feeding may represent a similar mechanism to control DTG malonylation percentage during the response to herbivore attack (Figure 2D). Using feed-back and -forward regulation together with differential expression levels of NaMaTs, plants maintain DTG malonylation percentage within a very narrow range. This is likely important because a malonylation percentage alteration as low as 4.1% in irAOC is associated with a drastically shortened style and infertility (Figure 6A). Additionally, the very low variation in the malonylation percentages reported here throughout the results indicates that DTG malonylation is precisely regulated. Although long-term, high-dose MeJA treatments of the leaves of VIGS plants (3 days using the same amount of MeJA normally applied to glasshouse-grown plants, with leaves typically 3-5x the size of the leaves of VIGS plants) reduced DTG malonylation percentages (VIGS-EV, Figure 4A and B), the locally transient endogenous JA bursts elicited by M. sexta larval feeding did not alter malonylation percentages (Figure 1E). Importantly, both high (irAOC) and low (VIGS-MaT1) malonylation percentages were accompanied by truncated styles. Notably, malonylation percentage decreased in irGGPPS-MaT1 inflorescences but without apparently affecting style length of irGGPPS-MaT1 plants (Figure 4—figure supplement 1B). We think that this is because irGGPPS plants produce much lower levels of DTGs, and thus the total abundance of DTGs in inflorescences may not be enough to affect style development, regardless of their malonylation.

Induction of the jasmonate signaling pathway, including via MeJA treatment and M. sexta attack, strongly induced NaMaT1 expression (Figure 2D) and DTG malonylation (Figure 1B), indicating that NaMaT1 is responsible for the increase in malonylated DTGs. However, as noted above, high-dose MeJA treatment suppressed malonylation percentages, and silencing JA biosynthesis (irAOC) increased malonylation percentage in many tissues (Figure 6A and Figure 6—figure supplement 1A and B). This apparent contradiction may be explained by the possibility that other MaTs also contribute to the DTG malonylation process, as indicated by the fact that M. sexta feeding suppresses NaMaT2 and NaMaT3 (Figure 2D). Although NaMaT1 transcript accumulation decreased more than 80% in VIGS-MaT1 leaves (Figure 3—figure supplement 1B), the malonylation percentage was only reduced by 19.6% (Figure 4B), again consistent with the hypotheses that other MaTs catalyze DTG malonylation. Future research could test NaMaT2 and NaMaT3 functions by manipulating their expression with more robust means, such as CRISPR-mediated genome editing.

Our experiments shed light on this phenomenon by demonstrating that the DTG biosynthesis specific NaGGPPS is required for the development of the truncated style phenotype (Figure 3), and this truncated style phenotype results from the low auxin levels found in the styles, which in turn are due to reduced IAA biosynthesis (Figure 5). We hypothesize that this style-specific effect occurs because the style synthesizes large amounts of DTGs (Figure 4—figure supplement 2C), and VIGS-MaT1 results in a stronger decrease in malonylation percentage in styles than it does in leaves (Figure 4B). In addition, styles contained the highest levels of IAA of all tissues analyzed (Figure 4—figure supplement 2) and are likely the auxin source for at least the gynoecium, as predicted by the apical-basal gradient of auxin theory (Nemhauser et al., 2000). Our data from irGGPPS plants with depleted DTGs supports our hypothesis that the truncated style of VIGS-MaT1 is related to DTGs, but the exact molecular events that lead to this phenomenon remain unknown. Comparing individual DTG patterns in VIGS plants in the irGGPPS, irAOC and EV backgrounds showed that changes of individual compounds are complex. As we do not know how plants perceive DTGs, it is very challenging to figure out which individual compound or combination of individual compounds could be perceived by plants and affect YUC activity. The low abundance and structural similarity of many DTGs, along with the instability of malonylation in solution ex vivo, make purification difficult (Heiling et al., 2016), and for the malonylated DTGs it is not feasible to obtain sufficient amounts or sufficient stability for the establishment and duration of bioassays. Furthermore, given the huge number of combinations of candidate DTGs, a gain-of-function test using specific DTGs is currently prohibitive. For example, if we were to try one or two DTGs at once, not accounting for isomers and limiting ourselves to the 16 DTG chemical formulae for which we could present relative quantification here, the total number of possible combinations is 2.8 × 10²⁵. This number of course could be restricted based on comparisons of the dynamics of individual compounds to the dynamics in malonylation percentage of styles in different treatment groups (EV, irAOC, irGGPPS; VIGS-EV vs. VIGS-MaT1), although the possibility that a ratio rather than a single compound is required could still result in many combinations that require testing.

The biosynthesis and malonylation of DTGs, which are diterpenoid derivatives, may interact with other compounds from this pathway, especially some phytohormones, like strigolactones, abscisic acid, cytokinins, gibberellins and brassinosteroids (Cazzonelli and Pogson, 2010). Notably, flavonoids were thus far the only known secondary metabolites that could inhibit auxin transport, resulting in stunted growth in Arabidopsis, Medicago, tomato and apple (Brown et al., 2001; Eckardt, 2006; Besseau et al., 2007; Schijlen et al., 2007; Dare et al., 2013), and malonyl-CoA is a required substrate for flavonoid biosynthesis (Kreuzaler and Hahlbrock, 1975). It is possible that silencing NaMaT1 may increase flavonoid biosynthesis, thereby affecting auxin and causing the short style phenotype. However, flavonoids did not significantly increase in VIGS-MaT1 plants (Figure 5—figure supplement 1A and B), and levels of rutin even decreased. Rutin has been reported not to affect auxin transport (Jacobs and Rubery, 1988). In summary, the short style phenotype is a malonylation-dependent phenotype that is based specifically on DTGs. Bioassay-driven metabolite extractions from VIGS-MaT1 tissues may help to discover the specific compound(s) inhibiting YUC activity.

In conclusion, this study reveals the uniformity of specialized metabolite malonylation and the importance of this uniformity: when this uniformity is disturbed by silencing a malonyltransferase gene and its regulator, JA signaling, the cells of the tissue which accumulates the highest levels of DTGs fail to elongate normally, resulting in a stunted style phenotype (Figure 7). This stunted style phenotype resulting from either JA signaling deficiencies or silencing NaMaT1, results from the inhibition of auxin biosynthesis. Elucidating how plants achieve this finely tuned DTG malonylation status, and which specific DTG structure is responsible for the inhibition of auxin biosynthesis in styles are exciting goals for future research. At a functional level, by shortening styles by titrating the degree of malonyl DTG decorations, plants may be able to regulate their outcrossing rates in response to environmental factors that influence JA signaling or DTGs accumulation, such as herbivory rates.

Figure 7

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All data generated or analysed during this study are included in the manuscript and supporting files

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Author details

1. Jiancai Li

   Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   Conceptualization, Data curation, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4417-7612

2. Meredith C Schuman

   1. Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
   2. Department of Geography, University of Zurich, Zurich, Switzerland

   Contribution

   Data curation, Formal analysis, Visualization, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3159-3534

3. Rayko Halitschke

   Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   Data curation, Visualization, Methodology, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1109-8782

4. Xiang Li

   Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   Validation, Investigation, Methodology

   Competing interests

   No competing interests declared

5. Han Guo

   Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   Validation, Investigation

   Competing interests

   No competing interests declared

6. Veit Grabe

   Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0736-2771

7. Austin Hammer

   Department of Biology, Brigham Young University, Provo, United States

   Contribution

   Validation, Investigation

   Competing interests

   No competing interests declared

8. Ian T Baldwin

   Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   Conceptualization, Resources, Data curation, Supervision, Funding acquisition, Visualization, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   baldwin@ice.mpg.de

   Competing interests

   Senior editor, eLife

   "This ORCID iD identifies the author of this article:" 0000-0001-5371-2974

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