Isoprenoid-derived plant signaling molecules: biosynthesis and biological importance
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The present review summarizes current knowledge of the biosynthesis and biological importance of isoprenoid-derived plant signaling compounds.
Cellular organisms use chemical signals for intercellular communication to coordinate their growth, development, and responses to environmental cues. The skeletons of majority of plant signaling molecules, mediators of plant intercellular ‘broadcasting’, are built from C5 units of isoprene and therefore belong to a huge and diverse group of natural substances called isoprenoids (terpenoids). They fill many important roles in nature. This review summarizes current knowledge of the biosynthesis and biological importance of a group of isoprenoid-derived plant signaling compounds.
KeywordsDimethylallyl diphosphate Isopentenyl diphosphate Isoprenoids Plant hormones Phytoecdysteroids Terpenoids
The terpenoids are a huge and structurally diverse group of natural substances formed from five-carbon (C5) units of isoprene (2-methyl-1,3-butadiene) via “head-to-tail” addition, as shown around 80 years ago by Ruzicka (1953), a Croatian chemist of Czech origin who was awarded the 1939 Nobel Prize in Chemistry for his work in this area. Compounds formed by combining isoprene units are now also known as isoprenoids. It is important to note that isoprenoids are found in all living organisms, including both eukaryotes (plants, animals, fungi) and prokaryotes (microorganisms). Although isoprene is a naturally occurring substance formed by the decomposition of various cyclic hydrocarbons, it is not itself a direct participant in terpenoid biosynthesis. Its biochemically active and biologically important forms are dimethylallyl diphosphate (DMAPP) and its isomer isopentenyl diphosphate (IPP). Various numbers of these C5 isoprenoid units can be combined to form linear monoterpenes (C10), diterpenes (C20), triterpenes (C30), tetraterpenes (C40) and polyterpenes (> C40) (Connolly and Hill 1992). These linear molecules often then undergo extensive intracellular modification, typically involving cyclization, oxidation, and rearrangement reactions. Several thousand isoprenoids have been identified to date, and new members of the family are regularly discovered. Studies on their biological effects have shown that they fill many different roles in nature, acting as attractants, repellents, hormones, growth inhibitors, pigments, and electron transport chain components (quinones). The most extensively studied essential isoprenoids are a family of tetracyclic triterpenoids known as sterols, which are found in both the animal and plant kingdoms, i.e. in most eukaryotes. The best-known sterol is cholesterol (C27), which can be produced by both plant and animal cells. Among other things, cholesterol is a key component of the lipid bilayer of animal cell plasma membranes (Singer and Nicolson 1972); it helps to maintain membranes’ semi-permeability and regulates their fluidity, which affects many transmembrane signaling processes. In vertebrates, it is also a precursor for the synthesis of steroid hormones and bile acids (Miller 1988; Javitt 1994). Notably, plant plasma membranes lack cholesterol and its fluidity is controlled by other plant sterols, phytosterols, which insert into a bilayer of phospholipids with their polar hydroxy groups close to the phospholipid head groups the similar way like cholesterol in animal plasma membrane (Cooper 2000). Leopold Ruzicka made important contributions to the characterization of metabolic pathways related to animal steroid hormones production, and showed that cholesterol can be modified to produce the male sex hormones androsterone (Ruzicka et al. 1934) and testosterone (Ruzicka and Wettstein 1935). The group of plant triterpenoids with steroidal skeletons includes plant signaling molecules such as brassinosteroids (BRs; C27–C29) and phytoecdysteroids (PEs; C27–C29), and over 250 different plant sterols (phytosterols; Piironen et al. 2000).
Other physiologically important terpenoid plant signaling molecules are the diterpenoid gibberellins (C19 and C20) and phytohormones derived from other isoprenoid compounds such as carotenoids (e.g. the strigolactones and abscisic acid) (Tholl 2015). Cytokinins (CKs) are adenine derivatives that can be modified at the N6 position with either isoprenoid or aromatic side chains to yield isoprenoid CKs (ISCK) or aromatic CKs (ARCK), respectively (Tarkowská et al. 2014). Two isoprenoid derivatives can form ISCK side chains: the C5 compound DMAPP (formed by the isomerization of IPP; Blackwell and Horgan 1993) and its hydroxylated analog 4-hydroxy-3-methyl-2-(E)-butenyl diphosphate (HMBPP; Krall et al. 2002). This review summarizes current knowledge of the biosynthesis of plant hormones formed from isoprenoid building blocks including their biological importance and their relationship to the two known biosynthetic pathways that produce the key C5 terpenoid building blocks, DMAPP and IPP, in plants: the mevalonate (MVA) and non-mevalonate pathways. The non-mevalonate pathway is also known as the 2-C-methyl-d-erythritol-4-phosphate (MEP) or the 1-deoxy-d-xylulose-5-phosphate pathway (DOXP), based on the name of the first or second intermediate formed, respectively.
Isoprenoid biosynthesis—the formation of C5 building blocks
In the 1990s, experiments using 13C- and 2H-labelled precursors (1-deoxy-d-xylulose) and analyses of the positions of the incorporated 13C atoms in newly formed isoprenoid carbon skeletons by gas chromatography–mass spectrometry (GC–MS) and nuclear magnetic resonance (NMR) revealed the existence of the mevalonate-independent IPP biosynthetic pathway (Rohmer et al. 1993; Schwender et al. 1996). In this alternative pathway, pyruvate and d-glyceraldehyde 3-phosphate (GAP) are the precursors of IPP that is used in the biosynthesis of plastidial isoprenoids. It was later shown that this pathway operates in most eukaryotic photosynthetic organisms such as higher plants, algae, prokaryotic cyanobacteria and eubacteria, but not in animals (Lichtenthaler 1998). The IPP formation pathway in plastids involves seven steps (Fig. 1). In the first step, GAP and pyruvate react to form 1-deoxy-d-xylulose 5-phosphate (DOXP; carbon C-2 of DOXP originating from pyruvate is inserted between carbon atoms 1 and 2 of GAP). The next reaction is an NADPH-dependent reductive conversion of DOXP into 2-C-methyl-d-erythritol 4-phosphate (MEP) via an intramolecular rearrangement (Schwender et al. 1999; Carretero-Paulet et al. 2002). The MEP and MVA pathways coexist in higher plants, but only the MEP pathway is active in many eubacteria and green algae.
Plant signaling molecules of isoprenoid origin
Studies on the model plant species Arabidopsis thaliana have shown that in addition to the early and late C-6 oxidation pathways, there may be an early C-22 oxidation side pathway for C28 BR biosynthesis and a C-23 hydroxylation shortcut (Fujioka et al. 2002; Ohnishi et al. 2006), as shown in Fig. 4.
The C27 BRs, which are counterparts of the C28 BRs lacking a methyl group at C-24 (norBRs), have the same carbon skeleton as cholesterol, which implies that they are synthesized from cholesterol in a similar way to the synthesis of CS from CR, i.e. via the late C-6 oxidation pathway (Kim et al. 2004) (Fig. 4). In addition, the C-24 methylation of norCS leading to the formation of CS in the presence of NADPH and S-adenosyl-l-methionine has been observed in a cell-free Arabidopsis enzyme extract (Joo et al. 2012).
Using a cell-free enzyme extract from rice seedlings, it was shown that C29 BRs, 24-ethyl BRs (so-called homoBRs), can be formed from sitosterol, a naturally abundant C29 phytosterol (Joo et al. 2015). In this case, homoCS is final biosynthetic product, and is generated via homoTE and homoTY (Fig. 4). Interestingly, no homoBL has been detected in plant tissues even though the analogous pathways discussed above terminate with the formation of BL itself or the corresponding analog. It also seems that C29 BRs can undergo C-28 demethylation to yield C28 BRs. Since C29 BRs are less biologically active than C28 BRs, this interconversion may allow plants to maintain a level of BR bioactivity that is optimal for various physiological processes.
Cytokinins (CKs) are another group of low molecular weight naturally-occurring substances that bind to specific receptors and thereby trigger cascades of reactions leading to the regulation of growth and development in planta. Among biologists, they are primarily known as the substances that control cell division (cytokinesis) in partnership with another hormone, auxin (Skoog and Armstrong 1970). They are also involved in lateral shoot formation, apical dominance, vascular differentiation, senescence, and other processes (Mok 1994).
Gibberellins (GAs) are a family of diterpenoid carboxylic acids with many natural sources. Although the first GAs were isolated from secretions of the fungus Gibberella fujikuroi (recently reclassified as Fusarium moniliforme) (Yabuta and Sumiki 1938) they are also present in several other fungal species and certain endophytic bacteria as well as in higher plants and some lower plants (Hedden and Thomas 2012). Since their discovery in the 1930s, over 130 gibberellins have been identified (http://www.phytohormones.info/gibberellins.htm). A few of these molecules are endogenous bioactive substances that control a wide range of plant growth and developmental processes including seed germination, stem elongation, flower initiation, and flower and fruit development. The major biologically active GAs are GA1, GA3, GA4, GA5, GA6 and GA7 (Yamaguchi 2008); other GAs found in plant tissues are typically biosynthetic precursors or metabolic products.
GAs have a tetracyclic skeleton consisting of either 19 or 20 carbon atoms (Fig. 2). Their de novo synthesis starts from GGDP, a common C20 diterpenoid precursor. It was initially believed that the isoprene units needed for GGDP formation originate from the MVA pathway (MacMillan 1998). However, recent studies using isotope-labelled precursors showed that it is actually the plastidial MEP pathway that provides most of the isoprene units for GA formation, and that the cytosolic MVA pathway’s contribution is minor (Kasahara et al. 2002).
Three cellular compartments are involved in GA biosynthesis—plastids, the endoplasmic reticulum (ER), and the cytosol. The GGDP formed in plastids is cyclized first into ent-copalyl diphosphate and then into volatile ent-kaurene (Urbanová et al. 2011). A loss of function of the genes encoding the enzymes catalyzing these two plastidial steps, ent-copalyl diphosphate synthase (EC 184.108.40.206) and ent-kaurene synthase (EC 220.127.116.11), produces GA-deficient phenotypes with extreme dwarfism and severe reproductive damage (non-germinating seeds, male and female infertility) (Koornneef and van der Veen 1980). The ent-kaurene then undergoes a series of oxidative transformations at carbon 19 catalyzed by ent-kaurene oxidase (EC 18.104.22.168) to produce ent-kaurenoic acid (KA) via ent-kaurenol and ent-kaurenal (Hedden and Thomas 2012). This enzyme is located in the outer membrane of the plastid (Rojas et al. 2001). The formation of GA12-aldehyde (GA12ald) requires a further two-step oxidation of KA at C-7β and C-6 by ent-kaurenoic acid oxidase (KAO; EC 22.214.171.124), which is present in the ER (Helliwell et al. 2001). Therefore, this step marks the point at which GA biosynthesis moves from the plastids to the ER. The transformation of GA12ald occurs via different pathways in fungi and plants, revealing a degree of independent pathway evolution. In fungi, GA12ald is oxidized by GA 3-oxidase (GA3ox) in the ER to form GA14-aldehyde (GA14ald) (Rojas et al. 2001). Conversely, in plants, KAO converts GA12ald into GA12, the substrate for KAO to provide GA12 precursor of all plant GAs (Hedden and Thomas 2012)—Fig. 6. The final reaction occurring in the ER in higher plants is an oxidation at C-13 mediated by GA 13-oxidase (GA13ox), which converts GA12 into its 13-hydroxylated analogue GA53. In fungi, the final step occurring in the ER is the formation of GA14 by the hydroxylation of GA14ald at C-7. The first part of the cytosolic phase of GA biosynthesis involves the formation of GA precursors via the sequential oxidation of C20-GAs at C-20 (i.e. at the methyl group attached to C-10) by GA 20-oxidases (GA20oxs). The second part then involves the introduction of a hydroxy functional group at C-3 of the GA structure by GA3ox to produce bioactive GAs. Importantly, GA20oxs catalyze the oxidative removal of C-20 from the C20-GAs skeleton. The mechanistic details of this process are currently unknown, but it produces C19-GAs with a γ-lactone bridge between C-19 and C-10 (Ward et al. 2002). The C-3 hydroxy group and the C-6 carboxyl group are essential for the biological activity of GA molecules (Harberd et al. 2009).
Phytoecdysteroids (PEs) are a group of about 300 compounds that are widely distributed but not ubiquitous in the plant kingdom (Tarkowská and Strnad 2016). Their role in plants is not completely clear, but there is some evidence that they may be endocrine disruptors that protect against plant-eating insects and/or soil nematodes (Bergamasco and Horn 1983; Kubo and Hanke 1986). Like BRs, they are tetracyclic triterpenoids with 27–29 carbon atoms, depending on the details of their biosynthesis. While there have been some studies on their biosynthesis, their formation has not been explored as thoroughly as that of BRs. What we know with some certainty is that the biosynthetic steps mirror those for BRs up to the point of squalene formation, and that the IPP used in their synthesis appears to originate from the MVA pathway, as in BR biosynthesis. However, this conclusion is based solely on the results of labelling experiments with 14C-mevalonic acid; none have yet been performed with 1-deoxy-d-xylulose (Grebenok and Adler 1993; Bakrim et al. 2008; Boo et al. 2010). Moreover, the only plant species considered in these studies have been spinach (Spinacia oleracea), a well-known source of PEs, and a perennial plant used in traditional Korean medicine (Achyranthes japonica). Both these species belong to the Amaranthaceae family. It was reported that 20-hydroxyecdysone (20E; Fig. 2), the most widely distributed PE, might be synthesized from a Δ7 sterol with a reduced side chain at C-24. This was confirmed by studies on spinach and related chenopods (Chenopodium album, Ch. quinoa), which showed that the sterol in question is lathosterol (Grebenok and Adler 1993; Xu et al. 1990). However, these plants also produce Δ5 sterols that may be alkylated (yielding C28–C29 sterols) or non-alkylated (yielding the C27 sterol cholesterol) at C-24. It is therefore unclear whether lathosterol or cholesterol is the preferred substrate for ecdysone 20-monooxygenase, which catalyzes the oxidation of ecdysone to 20E (Tarkowská and Strnad 2016).
The aim of this review was to place the biosynthesis of terpenoid plant hormones into the broader context of general terpenoid biosynthesis in plants. The authors also attempted to clearly identify the cellular compartments in which each biochemical process occurs, which is often neglected in scientific papers.
Author contribution statement
DT designed the outline of the article, composed the manuscript and figures. MS provided scientific feedback and critical comments and revised content. Both authors read and approved the manuscript.
Financial support from the Ministry of Education, Youth and Sport of the Czech Republic through the National Program of Sustainability (Grant no. LO 1204) is gratefully acknowledged. The authors would like to also express their sincere thanks to Sees-editing Ltd. for critical reading and editing of the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interests.
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