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Planta

, Volume 247, Issue 5, pp 1051–1066 | Cite as

Isoprenoid-derived plant signaling molecules: biosynthesis and biological importance

  • Danuše Tarkowská
  • Miroslav Strnad
Review

Abstract

Main conclusion

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.

Keywords

Dimethylallyl diphosphate Isopentenyl diphosphate Isoprenoids Plant hormones Phytoecdysteroids Terpenoids 

Abbreviations

ABA

Abscisic acid

BRs

Brassinosteroids

CKs

Cytokinins

DMAPP

Dimethylallyl diphosphate

DOXP

1-Deoxy-d-xylulose-5-phosphate pathway

GAs

Gibberellins

HMBPP

4-Hydroxy-3-methyl-2-(E)-butenyl diphosphate

IPP

Isopentenyl diphosphate

MEP

2-C-Methyl-d-erythritol-4-phosphate

MVA

Mevalonic acid

PEs

Phytoecdysteroids

SLs

Strigolactones

Introduction

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

As mentioned in the introduction, the first research on isoprenoid biosynthesis was conducted at the start of the twentieth century, when it was found that the carbon skeleton of terpenoid compounds consists of C5 units combined by head-to-tail addition. The first feeding experiments with isotopically labeled precursors were conducted in the early 1950s and focused on the biosynthesis of sterols (cholesterol in liver tissues and ergosterol in yeast). These studies revealed that cholesterol is made up from acetate units (activated in the form of acetyl coenzyme A, or acetyl-CoA; Little and Bloch 1950), which led to the discovery of the MVA pathway. Later, it was found that Claisen-type condensation of 2 molecules of acetyl-CoA followed by aldol condensation with a third (Fig. 1) yields the C6 compound S-3-hydroxy-3-methylglutaryl-CoA (HMG-CoA), which can then be reduced by NADPH to the essential intermediate MVA (Wolf et al. 1956). MVA is finally converted into IPP, the biological equivalent of isoprene, via three enzymatic steps including two ATP-dependent phosphorylations and one ATP-driven decarboxylation. After its discovery, the MVA pathway was universally accepted as the starting point for sterol biosynthesis, and thus for the biosynthesis of all natural isoprenoids. However, in the late 1950s, evidence from studies on isoprenoid biosynthesis in plants indicated that the MVA pathway may not be the only source of IPP. For instance, experiments using 14C-labelled MVA in maize yielded very low levels of incorporation into plastidial isoprenoids (β-carotene, phytol, etc.), whereas cytoplasmic sterols were quite rapidly labelled by the 14C-MVA (Goodwin 1958). Similar results demonstrating high labelling of cytoplasmic isoprenoid compounds and low labelling of plastidial isoprenoids were later obtained for various other plant species (e.g. carrot, tomato and oat) (Braithwaite and Goodwin 1960a, b; Lichtenthaler et al. 1982). Interestingly, isolated plastids could not make IPP from MVA (Lütke-Brinkhaus and Kleinig 1987), but 14C-labelled pyruvate and CO2 were rapidly incorporated (via photosynthesis in the latter case) into plastidial isoprenoids. These findings indicated that the MVA pathway does not operate in plastids, and that isoprenoid biosynthesis in these cell compartments does not rely on acetate-derived IPP.
Fig. 1

The biosynthesis of isoprenoids—the formation of C5 building blocks IPP and DMAPP by two distinct pathways in plants: mevalonate (taking place in cytosol) and methylerythritol phosphate pathway (taking place in plastids). Abbreviation of enzymes (marked in orange): AACT acetoacetyl-CoA thiolase, HMGS 3-hydroxy-3-methylglutaryl-CoA synthase, HMGR 3-hydroxy-3-methylglutaryl-CoA reductase, MK mevalonate kinase, PMK phosphomevalonate kinase, MPDC mevalonate diphosphate decarboxylase, IDI isopentenyl diphosphate isomerase, DXS 1-deoxy-d-xylulose 5-phosphate synthase, DXR 1-deoxy-d-xylulose 5-phosphate reductoisomerase, MCT (IpsD) 4-diphosphocytidyl-2-C-methyl-d-erythritol synthase, CMK (IspE) 4-diphosphocytidyl-2-C-methyl-d-erythritol kinase, MDS (IspF) 2-C-methyl-d-erythritol 2,4-cyclodiphosphate synthase, HDS (IspG) 4-hydroxy-3-methylbut-2-enyl diphosphate synthase, HDR (IspH) 4-hydroxy-3-methylbut-2-enyl diphosphate reductase

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

Abscisic acid

Abscisic acid (ABA; Fig. 2), which was first isolated in 1961 (Liu and Carns 1961), is one of the seven widely recognized groups of plant hormones with diverse roles as chemical messengers mediating cell–cell communication (Tarkowská et al. 2014). Its main roles are in regulating seed development (germination, maturation, dormancy), shoot elongation, root growth maintenance, and stomatal opening, and it is particularly important in processes relating to various environmental stresses (Patterson 2001; Nambara and Marion-Poll 2005). ABA is a non-volatile C15 terpenoid carboxylic acid, and at first glance, one might suspect that it is directly formed from the C15 sesquiterpene precursor farnesyl diphosphate (FDP). However, experiments with 18O-labeled precursors revealed that ABA is formed by the cleavage of C40 carotenoids originating from the MEP pathway (Milborrow and Lee 1998; Hirai et al. 2000)—Fig. 3. The ABA biosynthetic pathway can be divided into 3 stages, of which the first two occur in plastids and the last occurs in the cytosol. The first stage involves IPP formation via the MEP pathway; the second involves the synthesis and subsequent cyclization of linear isoprenoid intermediates; and the third involves the release of the C15 compound xanthoxin that is finally converted into ABA after two oxidative reactions. Briefly, IPP units are formed in the plastids from pyruvate and GAP, and then undergo head-to-tail addition to form successively C10 (geranyl diphosphate, GDP), C15 (FDP), and C20 (geranyl geranyl diphosphate, GGDP) molecules. Then, further head-to-head condensation of two GGPP units produces the C40 skeleton of the carotenoid phytoene, which undergoes four consecutive dehydrogenation reactions to form lycopene (C40H56). Lycopene can then be cyclized to either α- or β-carotene (Finkelstein 2013). Whereas α-carotene is used for lutein synthesis, β-carotene can be modified to the oxygenated carotenoid zeaxanthin, which is a direct precursor of ABA. Zeaxanthin, one of the most common carotenoid alcohols found in nature, is later converted to violaxathin (C40) by epoxidation (Fig. 3). As might be expected, mutant plants with impaired zeaxanthin epoxidase activity accumulate zeaxanthin and have greatly reduced ABA levels, leading to a phenotype producing non-dormant seeds (Koornneef et al. 1982; Marin et al. 1996; Agrawal et al. 2001). ABA biosynthesis then proceeds via the conversion of violaxanthin either directly to 9-cis-violaxanthin or to 9′-cis-neoxanthin via the formation of trans-neoxanthin (C40) (North et al. 2007; Neuman et al. 2014), which helps to protect plant tissues against photooxidative stress (Dall’Osto et al. 2007). The final plastidial step in ABA biosynthesis is the cleavage of both xanthins by 9-cis-epoxycarotenoid dioxygenase (NCED) to release the C15 compound xanthoxin (C15H22O3) into the cytosol; this is the rate-limiting step of ABA biosynthesis (Nambara and Marion-Poll 2005). In the cytosol, xanthoxin is first oxidized to abscisic aldehyde (C15H20O3) and then finally to abscisic acid (C15H20O4).
Fig. 2

Basic chemical structures of different classes of isoprenoid-derived plant signalling compounds or their prominent representatives

Fig. 3

The biosynthesis of abscisic acid. MoCo molybdenum cofactor. Abbreviation of enzymes: PSY phytoene synthase, ZEP zeaxanthin epoxidase, NSY neoxanthin synthase, NCED 9-cis-epoxycarotenoid dioxygenase, SDR short chain dehydrogenase/reductase, AAO abscisic aldehyde oxidase

Brassinosteroids

Brassinosteroids (BRs) are a group of plant signaling molecules with four-ringed steroidal skeletons that are classified as plant hormones (Caño-Delgado et al. 2004). They are important components of the hormonal network that controls various important physiological processes in the plant life cycle. During the reproductive phase of plant development, BRs are involved in germination, flowering and male fertility. In the vegetative growth phase, they regulate organ elongation, the timing of senescence, and plant tolerance to abiotic stresses (e.g. salinity, temperature, water) (Fujioka and Sakurai 1997). The first BR to be discovered was brassinolide (BL; Fig. 2), whose structure was elucidated in 1979 after its isolation from bee-collected Brassica napus pollen (Grove et al. 1979). Since the 1980s, over 70 BRs have been characterized (Bajguz 2011), but BL remains the most biologically active BR identified to date (Fujioka et al. 1995). In chemical terms, BRs (like many other plant sterols) are steroid alcohols. Structurally, they resemble cholesterol, the C27 predominant animal sterol. Depending on the substitution of their side chains (i.e. the nature of the C-24 alkyl substituent), BRs and other phytosterols may contain 27, 28, or 29 carbon atoms. However, C28 phytosterols such as BL are the most widespread in nature (Bajguz 2011). Unlike insects, which cannot cyclize the linear C30 hydrocarbon squalene, an essential precursor to the entire steroid family, plants and animals (including humans) possess a complete sterol biosynthetic pathway. The isoprenoid building blocks IPP and DMAPP used in BR synthesis originate from the cytosolic mevalonic acid pathway (Goldstein and Brown 1990). Mevalonate synthesis is the rate-limiting irreversible step in cholesterol biosynthesis, but the critical step in plant sterol biosynthesis seems to be the C-methylation of cycloartenol (a C30 Δ24 sterol formed by squalene cyclization) by sterol methyltransferase (SMT; EC 2.1.1.41). The rate of de novo plant sterol biosynthesis is thus limited by a post-squalene modification step in the biosynthetic pathway (Piironen et al. 2000)—Fig. 4. The complete plant sterol biosynthetic pathway involves a sequence of over 30 enzyme-catalyzed reactions leading to the Δ5-sterols sitosterol, cholesterol, and campesterol (CR), the latter of which is the first BR-specific biosynthetic precursor for C28 BRs bearing a methyl group at C-24. Extensive studies with various isotope-labelled intermediates revealed that CR is hydrogenated at ring B (C-6) in two steps to produce campestanol (CN), which is then transformed into castasterone (CS) and oxidized to produce the 7-oxolactone moiety of BL. These final transformations occur via two parallel pathways known as the early and the late C-6 oxidation pathways (Fujioka and Yokota 2003)—Fig. 4. Both pathways involve six oxidation reactions and converge with the formation of CS. In the early C-6 oxidation pathway, CN is converted into 6-oxocampestanol (6-oxoCN) and subsequently to cathasterone (CT; oxidation at C-22), teasterone (TE; oxidation at C-23), 3-dehydroteasterone (3DT; oxidation at C-3), typhasterol (TY; reduction at C-3), and finally CS (oxidation at C-2). In the late C-6 oxidation pathway, CN is first hydroxylated at C-22 to form 6-deoxocathasterone (6-deoxoCT), which is then converted into the C-6 deoxy analogs of the intermediates in the early C-6 oxidation pathway (Fig. 4). The high levels of some 6-deoxo biosynthetic intermediates found in certain plant species (Arabidopsis, pea, and tomato) suggest that the late C-6 pathway may be the dominant biosynthetic route to BRs (Nomura et al. 2001). However, these findings derive from studies that examined only a limited range of plant species; it would be interesting to evaluate this hypothesis further by testing a greater range of species.
Fig. 4

The scheme of biosynthesis of C27, C28 and C29 plant sterols with respect to brassinosteroids. Grey frame A—the initial steps of plant sterols biosynthesis. Grey frame B—the relation between the biosynthesis of C27, C28 and C29 plant sterols. Non-framed scheme—the biosynthesis of C28 brassinosteroids—the most widespread BRs in nature. Abbreviation of enzymes (marked in orange): IDI isopentenyldiphosphate isomerase, GDS geranyl diphosphate synthase, FDS farnesyl diphosphate synthase, SS squalene synthase, CAS cycloartenol synthase, SMT sterol methyltransferase. Abbreviation of selected compounds: CR campesterol, CN campestanol, CT cathasterone, TE teasterone, 3DT 3-deoxoteasterone, TY typhasterol, CS castasterone, BL brassinolide

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

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).

As mentioned in the introductory paragraph, CKs may have either an isoprenoid or an aromatic side chain at the N-6 position of their adenine moiety. Isoprenoid CKs (Fig. 2) can be formed in plant cells by the transfer of a donor C5 isoprenoid unit to an acceptor adenine molecule that may be either a free nucleotide (AMP, ADP, or ATP) or a tRNA-bound species (Frébort et al. 2011). The currently known viable isoprenoid donors are DMAPP and HMBPP. DMAPP may be formed via the MEP pathway in plastids or the MVA pathway in the cytosol of eukaryotes (Lichtenthaler 1999; Rohmer 1999). HMBPP is exclusively produced via the MEP pathway, which is active in plastids and bacteria (Hecht et al. 2001). The N-prenylation of adenine nucleotides is catalyzed by adenylate isopentenyltransferases (IPTs) (Takei et al. 2001), of which two types have been distinguished: (1) IPTs that add an isopentenyl unit to a free adenine nucleotide (EC 2.5.1.27) (Takei et al. 2001; Blackwell and Horgan 1993; Kakimoto 2001), and (2) IPTs that perform the same function for tRNA-bound adenine units (EC 2.5.1.8) (Persson et al. 1994). Reactions where DMAPP serves as the substrate of the IPT yield isopentenyladenine (iP) nucleotide as the primary product (Fig. 5). Conversely, reactions involving the hydroxylated isoprenoid substrate HMBPP yield trans-zeatin (tZ) nucleotide (Krall et al. 2002; Sakakibara et al. 2005). When a CK is formed from a tRNA-bound adenine nucleotide, the newly formed CK is released when the tRNA is degraded (Skoog et al. 1966). Contradicting early assumptions, this process was found not to be the primary source of CKs in plants; it now appears that it may account for only around 40% of total CK production due to the slow turnover of tRNA molecules (Klämbt 1992). However, tRNA degradation is a major source of cis-zeatin CKs (Vreman et al. 1978), i.e. CKs with a hydroxylated isoprenoid side chain in cis orientation (Fig. 5). Unlike its highly bioactive geometric isomer tZ, cis-zeatin (cZ) has little or no activity (Kudo et al. 2012). The relative abundance of the two zeatin stereoisomers can vary significantly over a plant’s lifecycle. Furthermore, tZ-type CKs are generally more abundant in unstressed tissues, while cZ-type CKs often dominate in tissues exposed to abiotic or biotic stress (Havlová et al. 2008; Pertry et al. 2009; Vyroubalová et al. 2009; Dobra et al. 2010). As shown by recent studies, the isoprenoid side chains of iP and tZ predominantly originate from the MEP pathway, whereas cZ side chains originate from the MVA pathway (Kasahara et al. 2004).
Fig. 5

The biosynthesis of isoprenoid cytokinins. Abbreviation of enzymes: IPT adenylate isopentenyltransferase, CYP450 cytochrome P450 monooxygenase, ZR zeatin reductase. Abbreviation of compounds: AMP adenosine monophosphate, ADP adenosine diphosphate, ATP adenosine triphosphate, DMZMP dihydrozeatin riboside-5′-monophosphate, DMAPP dimethylallyl diphosphate, HMBPP 4-hydroxy-3-methyl-2-(E)-butenyl diphosphate, iPMP isopentenyladenosine-5′-monophosphate, iPDP isopentenyladenosine-5′-diphosphate, iPTP isopentenyladenosine-5′-triphosphate, PPi diphosphate, tRNA transfer ribonucleic acid, tZMP trans-zeatin riboside-5′-monophosphate, tZDP trans-zeatin riboside-5′-diphosphate, tZTP trans-zeatin riboside-5′-triphosphate

Gibberellins

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).

The first steps of GA biosynthesis are the same as those of ABA biosynthesis, i.e. C5 isoprenoid units are formed in plastids via the MEP pathway and combined by head-to-tail addition to produce the linear isoprenoids GPP, FDP, and finally GGDP (Urbanová et al. 2011)—Fig. 6. The importance of the MEP pathway in GA and ABA biosynthesis was proven by experiments with plants in which the normal transformation of 1-deoxy-d-xylulose 5-phosphate into the branched compound 2-C-methyl-d-erythritol 4-phosphate (MEP) by 1-deoxy-d-xylulose 5-phosphate reductoisomerase (DXR; EC 1.1.1.267) was disrupted. This caused deficiencies in the biosynthesis of gibberellin (producing a dwarf phenotype) and abscisic acid (producing a stomatal closure defect), together with a biosynthetic deficiency of photosynthetic pigments (leading to an albino phenotype) (Xing et al. 2010). Moreover, the IPP/DMAPP flux from the cytosolic MVA pathway was insufficient to rescue the deficiency caused by impairment of the plastidial MEP pathway. Similarly, it was revealed that the activity of 1-deoxy-d-xylulose-5-phosphate synthase (DXS; EC 2.2.1.7), the first enzyme of the MEP pathway, is rate-limiting for IPP production and that the biosynthesis of GAs and other isoprenoid molecules including ABA is impaired in albino mutant plants (Estévez et al. 2000; García-Alcázar et al. 2017).
Fig. 6

The biosynthesis of gibberellins in plants. The frame filled in with grey colour represents the comparison of the GAs biosynthetic pathway in the fungus Gibberella fujikuroi and plants. ER endoplasmic reticulum. Abbreviation of enzymes: IDI isopentenyldiphosphate isomerase, GDS geranyl diphosphate synthase, FDS farnesyl diphosphate synthase, GGDS geranyl geranyl diphosphate synthase, CPS ent-copalyl diphosphate synthase, KS ent-kaurene synthase, KO ent-kaurene oxidase, KAO ent-kaurenoic acid oxidase, DES 1,2-desaturase, GA13ox GA 13-oxidase, GA20ox GA 20-oxidase, GA3ox GA 3-oxidase

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 5.5.1.13) and ent-kaurene synthase (EC 4.2.3.19), 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 1.14.13.78) 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 1.14.13.79), 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

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).

Strigolactones

Strigolactones (SLs) are the most recently discovered group of plant signaling molecules exhibiting hormonal activity. Their discovery was largely due to their apparent role in inhibiting shoot branching (Gomez-Roldan et al. 2008; Umehara et al. 2008), which appears to be regulated by a mechanism involving interplay between SLs, CKs, and auxins. SLs also appear to regulate leaf senescence together with the gaseous hormone ethylene (Ueda and Kusaba 2015), and to control other physiological process such as the balance of resource distribution via strategic modification of growth and development. For instance, phosphate deprivation induced plants to increase their SL biosynthesis, leading to changes in root growth and the promotion of fungal symbiosis (suggesting that some SLs function as rhizosphere signaling molecules) to increase phosphate intake (Brewer et al. 2013). To date, around 20 SLs have been identified in root exudates from various terrestrial plants and chemically characterized (Al-Babili and Bouwmeester 2015). They are tricyclic lactones with three fused rings designated A, B and C, and a butenolide ring (D) that is attached via an enol ether bond (Zwanenburg et al. 2009). They appear to be synthesized via a carotenoid pathway like ABA (see above). Accordingly, their biosynthesis begins in the plastids, with the formation of the C5 building blocks IPP and DMAPP via the MEP pathway, and continues with the production of carlactone (CL), a specific SL precursor substance with a SL-like carbon skeleton containing rings A and D (see Fig. 7). CL is derived from β-carotene via a process similar to that which produces the ABA precursor zeaxanthin. Specifically, its formation was shown to involve the isomerization of trans-β-carotene to 9-cis-β-carotene (C40H56), which is then cleaved to yield the C19 compound (Z)-CL, in which the C9–C10 bond has the cis-geometry and the C-11 stereocenter has the R-configuration (Alder et al. 2012; Bruno et al. 2014; Seto et al. 2014). These reactions are catalyzed by CAROTENOID CLEAVAGE DIOXYGENASE 7 (CCD7; EC 1.13.11.68) and CAROTENOID CLEAVAGE DIOXYGENASE 8 (CCD8; EC 1.13.11.691). The biosynthetic process then shifts from the plastids to the cytosol (Lopez-Obando et al. 2015), where (Z)-CL undergoes further stereoselective oxidation and cyclization reactions to form the BC lactone moiety. While the mechanisms of these reactions remain to be determined and the associated enzymes have yet to be identified, it is believed that the cytochrome P450 monooxygenase may be involved (Alder et al. 2012; Seto et al. 2014; Booker et al. 2005). With regard to the configuration of the natural SL skeleton, two types of SL diastereoisomers can be recognized: strigol-type and orobanchol-type. These types differ in terms of the configuration of the B–C-ring junction but both have the R-configuration at the C-2′ position. It is believed that 5-deoxystrigol is the precursor of strigol-type SLs while ent-2′-epi-5-deoxystrigol is the direct biosynthetic precursor of orobanchol-type SLs (Fig. 7).
Fig. 7

The biosynthesis of strigolactones. Abbreviation of enzymes: PDS phytoene desaturase, LYC lycopene cyclase, CAI (D27) all trans/9-cis-β-carotene isomerase, CCD7 carotenoid cleavage dioxygenase 7, CCD8 carotenoid cleavage dioxygenase 8 (carlactone synthase), MAX1 a cytochrome P450

Conclusion

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.

Notes

Acknowledgements

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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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Growth Regulators, Faculty of Science, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany AS CRPalacký UniversityOlomoucCzechia

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