The decoration of specialized metabolites influences stylar development

Abstract

Plants produce many different specialized (secondary) metabolites that function in solving ecological challenges; few are known to function in growth or other primary processes. 17-Hydroxygeranylinalool diterpene glycosides (DTGs) are abundant herbivory-induced, structurally diverse and commonly malonylated defense metabolites in Nicotiana attenuata plants. By identifying and silencing a malonyltransferase, NaMaT1, involved in DTG malonylation, we found that DTG malonylation percentages are normally remarkably uniform, but when disrupted, result in DTG-dependent reduced floral style lengths, which in turn result from reduced stylar cell sizes, IAA contents, and YUC activity; phenotypes that could be restored by IAA supplementation or by silencing the DTG pathway. Moreover, the Nicotiana genus-specific JA-deficient short-style phenotype also results from alterations in DTG malonylation patterns. Decorations of plant specialized metabolites can be tuned to remarkably uniform levels, and this regulation plays a central but poorly understood role in controlling the development of specific plant parts, such as floral styles.

The Phytotoxicity of Meta-Tyrosine Is Associated With Altered Phenylalanine Metabolism and Misincorporation of This Non-Proteinogenic Phe-Analog to the Plant's Proteome

“…Primary metabolites that are associated with essential cellular functions, e.g., nucleotides, amino acids, fatty acids, sugars, and organic acids, which are typically present in all organisms and cells. In addition, organisms also produce numerous specialized (secondary) metabolites that are not essential to basic physiological functions, but otherwise play important roles during specific growth and developmental stages, and aid in adapting and adjusting the developmental need of the plant with specific physiological or environmental signals (Witzany, 2006;Tissier et al, 2014;Moghe and Last, 2015;Wurtzel and Kutchan, 2016;Li et al, 2018). Specialized compounds produced in plants were shown to have key roles in defense mechanisms, in inter-or intracellular signaling, coloring, regulation of primary metabolism, as well as in allelochemisrty (i.e., biomolecules produced by one organism that have a physiological effect on another species when released to the environment) (Rizvi and Rizvi, 1992).…”

Specific decorations of 17-hydroxygeranyllinalool diterpene glycosides solve the autotoxicity problem of chemical defense inNicotiana attenuata

“…The impressive structural diversity of HGL-DTGs in N. attenuata plants results largely from glycosylation and malonylation reactions. While all malonyl decorations are instantaneously lost in the alkaline pH environment of the midgut of M. sexta larvae and therefor may play more important roles in planta (Poreddy et al, 2015;Li et al, 2018), glycosylation leads to a constant and stable pool of potential defensive compounds. Larvae feeding on leaf disks of transgenic IRggpps plants grow larger than larvae feeding on WT leaves, indicating that the overall abundance of HGL-DTGs is a major factor of the plant's resistance against M. sexta (Figure 9), consistent with earlier studies (Jassbi et al, 2008;Heiling et al, 2010;Jassbi et al, 2010).…”

“…However, the enzymes necessary for further hydroxylation and glycosylation steps, which determine most of the structural diversity of HGL-DTGs, remain to be characterized. Li and colleagues (Li et al, 2018) identified and silenced a malonyltransferase (NaMAT1), which is responsible for the malonylation of HGL-DTGs. However, all malonyl moieties of HGL-DTGs are rapidly lost when leaves are ingested by M. sexta larvae, suggesting that the malonylation of HGL-DTGs does not play a central role in anti-herbivore defense (Poreddy et al, 2015).…”

“…However, all malonyl moieties of HGL-DTGs are rapidly lost when leaves are ingested by M. sexta larvae, suggesting that the malonylation of HGL-DTGs does not play a central role in anti-herbivore defense (Poreddy et al, 2015). Interestingly, disruption of the uniform malonylation patterns of HGL-DTGs leads to a specific reduction in the floral style lengths of N. attenuata flowers (Li et al, 2018). This shows that specific decorations of a plant's specialized metabolites can play a crucial, but poorly understood, role in plant development.…”

In Search of Bioactivity – Phyllobilins, an Unexplored Class of Abundant Heterocyclic Plant Metabolites from Breakdown of Chlorophyll

“…Tagging of natural products is often involved in signaling for the plant, e. g. in response to attack by herbivores, such as insects. Malonylation of secondary metabolites from Nicotiana attenuata , the 17‐hydroxygeranyl‐linalool diterpene glycosides (DTGs), was found to increase upon insect feeding, a response that is thought not to act as defense mechanism, since the malonyl residues were demonstrated to be removed upon ingestion in herbivores, suggesting a different role . Malonylated PBs have been identified, amongst others, in Nicotiana rustica and Brassica napus .…”