Genetic aspects of auxin biosynthesis and its regulation

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eGenetic aspects of auxin biosynthesis and its regulation

Javier Brumos, Jose M. Alonso and Anna N. Stepanova*

Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695,

USA

*Corresponding author, e-mail: [email protected]

Received 30 May 2013; revised 30 July 2013

Auxin is an essential plant hormone that controls nearly every aspect of a plant’s life, from embryo

development to organ senescence. In the last decade the key genes involved in auxin transport,

perception, signaling and response have been identified and characterized, but the elucidation of auxin

biosynthesis has proven to be especially challenging. In plants, a significant amount of indole-3-acetic

acid (IAA), the predominant biologically active form of auxin, is synthesized via a simple two-step

route where indole-3-pyruvic acid (IPyA) produced from L-tryptophan by TAA1/TAR

aminotransferases is converted to IAA by the YUC family of flavin monooxygenases. The TAA1/TAR

and YUC gene families constitute the first complete auxin biosynthetic pathway described in plants.

Detailed characterization of these genes’ expression patterns suggested a key role of local auxin

biosynthesis in plant development. This has prompted an active search for the molecular mechanisms

that regulate the spatiotemporal activity of the IPyA route. In addition to the TAA1/TAR and YUC-

mediated auxin biosynthesis, several alternative routes of IAA production have been postulated to

function in plants, but their biological significance is yet to be demonstrated. Herein, we take a genetic

perspective to describe the current view of auxin biosynthesis and its regulation in plants, focusing

primarily on Arabidopsis.

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/ppl.12098

This article is protected by copyright. All rights reserved.

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eAbbreviations – AAO, aldehyde oxidases; ABA, abscisic acid; AMI1, indole-3-acetamide hydrolase;

CAM, camalexin; ChIP, chromatin immunoprecipitation; CYP71A13, indoleacetaldoxime

dehydratase; CYP79B2/B3, cytochrome P450 monooxygenases; IAA, indole-3-acetic acid; iaaH,

indole-3-acetamide hydrolase; IAAld, indole-3-acetaldehyde; iaaM, tryptophan monooxygenase;

IAM, indole-3-acetamide; IAN, indole-3-acetonitrile; IAOx, indole-3-acetaldoxime; IGs, indole

glucosinolates; IGP, indole-3-glycerol phosphate; IPyA, indole-3-pyruvic acid; KYN, kynurenine;

LEC2, leafy cotyledon2; MYR, myrosinases; NGAs, NGATHA; NITs, nitrilases; PDC, pyruvate

decarboxylases; PIFs, phytochrome interacting factors; PLT, plethora; STY1, short-

internodes/Stylish1; SUR1, alkylthiohydroximate C-S lyase; SUR2, cytochrome P450 monooxygenases

CYP83B1; TAA1/TARs, tryptophan aminotransferases; TAM, tryptamine; Trp, tryptophan; UGT74B1,

UDP-glucose:thiohydroximate S-glucosyltransferase; VAS1, aminotransferase, suppressor of TAA1-

SAV3; WEI2/WEI7, anthranilate synthases ASA1 and ASB1; YUCs, YUCCAs.

Introduction Since the discovery of the first plant hormone in the 1930s (Thimann and Koepfli 1935), auxin indole-

3-acetic acid (IAA), its regulatory roles and molecular mechanisms of action have become the research

focus for many plant biologists. Over the years, numerous reports of the crucial involvement of this

hormone in every stage of a plant’s life cycle have flooded scientific literature. Despite this massive

research effort, our current understanding of how this hormone is made remains fragmentary.

Nevertheless, new genetic, biochemical and pharmacological approaches, together with the

development of more sensitive methods for auxin metabolites’ quantification, are starting to shed fresh

light on this challenging biosynthetic pathway.

Based primarily on biochemical approaches, two general pathways for IAA biosynthesis have

been proposed: the tryptophan (Trp) dependent and the Trp-independent routes (Figure 1) (Normanly

et al. 1993). The Trp-independent route is thought to branch out from the L-Trp biosynthetic pathway

at the level of indole and/or indole-3-glycerol phosphate (Ouyang et al. 2000). Despite considerable

biochemical evidence supporting the existence of this route, very little is known about the enzymatic

reactions, metabolic intermediates and genes involved (Östin et al. 1999). A putative cytosolic indole

synthase homologous to the plastidic AtTSA1 has been suggested as the first component of this elusive

pathway (Zhang et al. 2008), but compelling physiological, biochemical or genetic evidence has not

yet been reported to convincingly demonstrate the involvement of this gene in IAA biosynthesis.

In contrast with the Trp-independent route, some of the Trp-dependent pathways are much better

characterized and specific enzymatic reactions, metabolites and genes have been firmly or, in some

cases, tentatively implicated in Trp-dependent auxin biosynthesis in plants. Backed by variable

amounts of experimental support, at least three Trp-dependent routes have been proposed: the indole-

3-acetaldoxime (IAOx), indole-3-acetamide (IAM) and the indole-3-pyruvic acid (IPyA) routes.

Herein, we review the evidence in support of each of the postulated pathways, and outline future work


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enecessary to confirm, complete and/or determine the role of the postulated players in IAA production.

Finally, we examine the current understanding of the regulation of auxin biosynthesis and its critical

importance in plant development and environmental responses.

The indole-3-acetaldoxime (IAOx) pathway The IAOx route is believed to be largely restricted to the Brassica genus (Sugawara et al. 2009). In

Arabidopsis thaliana the cytochrome P450 monooxygenases CYP79B2 and CYP79B3 catalyze the

conversion of Trp to IAOx (Zhao et al. 2002, Sugawara et al. 2009). The bulk of IAOx produced is

typically used in the synthesis of secondary metabolites, such as indole glucosinolates and camalexins

(reviewed in Bender and Celenza 2009). Nevertheless, lines of experimental evidence also point to a

potential role of this pathway in the biosynthesis of auxin. Thus the cyp79b2 cyp79b3 double mutants

that are unable to make IAOx display shorter hypocotyls and lower IAA content at high temperatures

as compared to wild type. However, under standard growth conditions these mutants exhibit very

subtle growth defects, suggesting that the IAOx pathway may contribute to the production of IAA only

under specific conditions (Zhao et al. 2002). On the other hand, when the conversion of IAOx into

indole glucosinates is blocked by means of genetic mutations, such as superroot1 (sur1), sur2, or

UDP-glucosyltransferase74b1 (ugt74b1), high auxin levels accumulate (Bak et al. 2001, Grubb et al.

2004, Mikkelsen et al. 2004). Although the flow of metabolites from IAOx to IAA is not fully

understood, two potential intermediates have been identified, indole-3-acetamide (IAM) and indole-3-

acetonitrile (IAN) (Sugawara et al. 2009). In vitro enzymatic assays indicate that CYP71A13 may be

responsible for the conversion of IAOx into IAN (Nafisi et al. 2007). In vivo, biosynthesis of the

IAOx-derived camalexins (see Figure 1), which is disrupted in the cyp71a13 mutant, is restored upon

exogenous IAN application, further implicating CYP71A13 in the production of IAN from IAOx.

Consistent with this idea is the accumulation of IAN upon ectopic co-expression of the Arabidopsis

CYP79B2 and CYP71A13 in Nicotiana benthamiana, a species that lacks equivalent enzymes and does

not normally produce detectable levels of IAOx or IAN (Nafisi et al. 2007). Taken together these

results imply that CYP71A13 can catalyze the conversion of IAOx to IAN (Nafisi et al. 2007), but it

remains to be determined whether or not the IAN produced via this pathway has a significant

contribution to the total IAA content in wild-type Arabidopsis.

In addition to the synthesis of IAN via the CYP79B2-CYP71A13 pathway, IAN can also be made

upon hydrolysis of indole glucosinolates by myrosinases (Searle et al. 1982). In this case IAN and

other nitriles are believed to function primarily in plant defense responses against biotic stresses

(reviewed in Hansen and Halkier 2005), while the role of this route in the production of IAA is

currently unknown. One proposed mechanism for the conversion of IAN into IAA involves a group of

enzymes called nitrilases (NITs) (Bartling et al. 1992, Bartel and Fink 1994) (Figure 1). In

Arabidopsis, the first molecular and biochemical evidences for the existence of NITs were obtained by

Bartling and co-authors (Bartling et al. 1992, Bartling et al. 1994) and additional genetic evidences


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efrom a mutant screen for plants resistant to exogenous IAN implicated these enzymes in IAA

production (Bartel and Fink 1994). There are four NITs in the Arabidopsis genome that could, in

principle, catalyze the hydrolysis of IAN to IAA. In vitro experiments, however, indicate that the IAN

hydrolysis by these nitrilases is highly inefficient (Vorwerk et al. 2001) and can also produce IAM in

addition to IAA (Pollmann et al. 2002). NIT1, NIT2 and NIT3 have been found to exhibit a strong

substrate preference towards phenylpropionitrile, allylcyanide, phenylthio acetonitrile, and methylthio

acetonitrile, suggesting that the primary role for these NITs is the conversion of nitriles derived from

indole glucosinolate turnover to carboxylic acids rather than IAA production (Vorwerk et al. 2001).

NIT4, on the other hand, has been shown to function in cyanide detoxification where it hydrolyses ß-

cyanoalanine to aspartic acid and ammonia (Piotrowski et al. 2001). Consistent with the idea that IAN

is not exclusively involved in auxin biosynthesis, the levels of IAN in Arabidopsis tissues are in fact

two orders of magnitude higher than those of IAA (Sugawara et al. 2009, Novák et al. 2012) and the

overexpression of NIT2 does not lead to auxin overproduction phenotypes (Normanly et al. 1997).

This further reinforces the idea that IAN and NITs may not participate in the production of IAA in a

significant way, but rather play a preponderant role in glucosinolate metabolism, camalexin

homeostasis, and cyanide detoxification (Su et al. 2011). Nonetheless, current state of knowledge does

not fully eliminate the possibility of the involvement of the IAOx pathway in the production of IAA.

In fact, the morphological and metabolic phenotypes of the sur1, sur2 and ugt74b1 mutants suggest

that a balance between the production of defense compounds and IAA is maintained in wild-type

plants. This raises the possibility that under specific developmental or environmental conditions the

IAOx pathway can make a significant contribution to free IAA pools.

The indole-3-acetamide (IAM) pathway The IAM pathway was previously believed to be present only in auxin-synthesizing bacteria. In

Agrobacterium, for example, this pathway is represented by two genes, iaaM and iaaH. The iaaM

gene encodes a tryptophan monooxygenase that converts TRP to IAM, whereas the indole-3-

acetamide hydrolase iaaH catalyzes the synthesis of IAA from IAM (Figure 1). The existence of an

equivalent IAM pathway in plants has been proposed (Pollmann et al. 2003). This possibility is

supported by the identification of IAM as an endogenous compound in several plant species (Pollmann

et al. 2002, Sugawara et al. 2009, Novák et al. 2012). In Arabidopsis, IAM is mainly produced from

IAOx (Sugawara et al. 2009). Consistent with this, IAM levels are significantly decreased in the

cyp79b2 cyp79b3 double mutants (Sugawara et al. 2009) defective in the conversion of Trp to IAOx

(Mikkelsen et al. 2000, Zhao et al. 2002). Feeding of the double mutants with 13C6-labelled IAOx,

leads to the production of 13C6-labelled IAM and IAN (Sugawara et al. 2009), suggesting that both

IAM and IAN can be generated in plants from the precursor IAOx. It is important to indicate,

however, that IAM has also been identified in several other plant species not belonging to the Brassica

genus that cannot make IAOx, raising the possibility that IAM can also be generated in an IAOx-


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eindependent way (Sugawara et al. 2009).

The big question remains of how IAM and IAN are produced from IAOx and how these

compounds are then converted into IAA. Overexpression of the bacterial iaaM gene or feeding of

wild-type plants with exogenous IAM lead to high in planta levels of auxin (Klee et al. 1987),

suggesting that Arabidopsis possesses the endogenous enzymatic activity required for the conversion

of IAM to IAA. In fact, amidase genes with sequence similarity to the bacterial gene iaaH/aux2/tms2

have been identified in several plant species (Pollmann et al. 2003, Nemoto et al. 2009). The

enzymatic activity towards IAM has been demonstrated in vitro for AtAMI1 and in cell culture for

NtAMI1. Thus, the identification and preliminary characterization of AtAMI1 have opened new

avenues to investigating the IAM pathway at the genetic level. Thorough morphological, genetic and

metabolic characterization of loss- and gain-of-function AtAMI1 mutant lines will be necessary to

firmly establish the role of this gene in IAA production in plants. Another key aspect awaiting

experimental clarification is the possible metabolic and genetic interconnection between the IAOx and

IAM pathways (Figure 1) that, as indicated above, share some of their intermediate metabolites.

The indole-3-pyruvic acid (IPyA) pathway Several recent studies have shown that most of IAA in plants is produced through the IPyA pathway

(Mashiguchi et al. 2011, Stepanova et al. 2011, Won et al. 2011). Originally, based on bacterial

models, a three-step IPyA route was postulated: aminotransferases convert Trp to IPyA, which is then

decarboxylated into indole-3-acetaldehyde (IAAld) and oxidized into IAA. The identification and

characterization of TAA1, TAR1 and TAR2 aminotransferases in Arabidopsis (Stepanova et al. 2008,

Tao et al. 2008, Yamada et al. 2009) provided strong support for the first step of this pathway (i.e. the

conversion of Trp into IPyA). Mutations in TAA1 and TARs lead to reduced levels of IAA (Stepanova

et al. 2008, Tao et al. 2008), as well as IPyA (Mashiguchi et al. 2011). Furthermore, purified TAA1 or

TARs are able to convert Trp into IPyA in vitro (Stepanova et al. 2008, Tao et al. 2008). Finally,

plants overexpressing TAA1 also show an increase in the IPyA levels (Mashiguchi et al. 2011, Novák

et al. 2012).

In contrast with the strong experimental support for the aminotransferase step, the situation was

much more complicated for the proposed subsequent conversion of IPyA into IAAld and then into

IAA. On the one hand, consistent with the original model, IAAld treatments lead to increased IAA

levels (Larsen 1949), putative pyruvate decarboxylases (PDC) and aldehyde oxidases (AAO) are

present in the Arabidopsis genome (Ye and Cohen 2009, Stepanova et al. 2011, Sekimoto et al. 1998),

and AAO activity is detectable in Arabidopsis extracts (Seo et al. 1998). On the other hand, detailed

biochemical and genetic analysis of all four putative AtPDC genes ruled out any significant role for

these genes in auxin biosynthesis (Stepanova et al. 2011, Ye and Cohen 2009). Several double and

triple pdc mutant combinations and four different pdc triple mutant combinations in the sensitized taa1

mutant background failed to show any effect on auxin-related phenotypes (Stepanova et al. 2011).


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eSimilarly, the role of the four AtAAO enzymes in IAA synthesis is uncertain. The aba3 mutant, which

does not produce molybdenum cofactor and therefore does not have any aldehyde oxidase activity,

does not display any obvious auxin-related developmental defects nor accumulates IAAld, suggesting

that aldehyde oxidases do not play a significant role in auxin biosynthesis (Mashiguchi et al. 2011).

Furthermore, some of the AtAAOs are known to be involved in abscisic acid biosynthesis (Seo et al.

2000). Thus, in the absence of direct in planta evidence for the role of the predicted AtPDCs and

AtAAOs in the IPyA pathway, the support for an IPyA model resembling the bacterial IPyA pathway

has been significantly weakened. In other words, while the production of IAA via IPyA is well-

supported experimentally, the mechanism by which IPyA is then converted into IAA remained

elusive.

The solution to this dilemma came from the genetic and biochemical analyses of a previously

identified auxin biosynthetic family of YUCCA (YUC) flavin monooxygenases in Arabidopsis.

Originally identified in an activation tag genetic screen, the gain-of-function yuc mutants were shown

to produce high levels of IAA. Biochemical studies suggested that YUCs worked in the so-called

tryptamine (TAM) pathway, where Trp was decarboxylated to TAM by the tryptophan decarboxylases

(TDCs), hydroxylated to N-hydroxytryptamine by YUCs, and finally converted to IAOx, thus merging

at this point with the IAOx pathway (Zhao et al. 2001). In recent years, however, experimental

evidences started to mount against this model. The first data contradicting this model came from the

findings that TAM was not metabolized in plants to produce IAA (Quittenden et al. 2009). Shortly

after, YUCs’ ability to catalyze the hydroxylation of TAM was also questioned (Zhao 2010, Tivendale

et al. 2010, Ross et al. 2011). Finally, experimental evidence indicating that TDCs participate in indole

alkaloid and serotonin rather than IAA biosynthesis (Lehmann and Pollmann 2009, Gutensohn et al.

2011) further weakened the involvement of YUCs in the putative TAM pathway.

The first clue to YUCs and TAA1/TARs working in the same route of auxin biosynthesis came

from the phenotypic comparison of the corresponding mutants (Mashiguchi et al. 2011, Stepanova et

al. 2011, Won et al. 2011). The IAA levels in the quadruple yuc1/2/4/6 mutants are similar to those of

the taa1 tar2 doubles and are much lower than that of wild-type plants. More importantly, this drop in

IAA in the mutants leads to nearly indistinguishable growth and developmental defects, including

abnormal meristem function, gravitropic response, lateral root formation, vasculature patterning and

floral development (Mashiguchi et al. 2011, Stepanova et al. 2011, Won et al. 2011). Furthermore the

taa1 tar2 mutant phenotypes can be phenocopied by certain yuc mutant combinations. For instance,

roots of the yuc3 yuc5 yuc7 yuc8 yuc9 quintuple mutants like that of taa1 tar2 are resistant to ethylene

and NPA, and yuc1 yuc4 doubles show shade avoidance defects similar to that of taa1 (Won et al.

2011). Another piece of evidence in support of YUCs and TAA1/TARs functioning in the same

pathway of auxin biosynthesis came from an experiment that utilized a potent chemical inhibitor of

TAA1 and TARs, kynurenine (Kyn) (He et al. 2011). Kyn treatments blocked IPyA production in vitro

and fully suppressed all of the high-auxin phenotypes of YUC1 overexpression lines, suggesting that


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eauxin biosynthesis via YUCs requires functional TAA1 and TARs and thus implying sequential action

of the two families in a single route (Stepanova et al. 2011). Consistent with this model, taa1 tar2

doubles exhibited a major decrease in IPyA levels, whereas yuc1 yuc2 yuc6 triples had an elevated

content of IPyA (Mashiguchi et al. 2011, Won et al. 2011). Conversely, estradiol-inducible YUC6ox

lines showed a drop in IPyA but a spike in IAA levels (Mashiguchi et al. 2011). Furthermore,

synergistic effects on auxin production were observed in transgenic plants co-expressing both the

TAA1ox and the YUC6ox constructs (Mashiguchi et al. 2011). Finally, purified YUC2 was shown to

catalyze the conversion of IPyA into IAA in vitro (Mashiguchi et al. 2011).

In summary, the key IPyA pathway of auxin production has turned out to be simpler than initially

thought: IPyA is produced from Trp by the tryptophan aminotransferases TAA1/TARs (SAV3, Shade

Avoidance3, Tao et al. 2008; WEI8, Weak Ethylene Insensitive8, Stepanova et al. 2008; TIR2,

Transport Inhibitor Response2, Yamada et al. 2009) and is then converted to IAA by the YUC family

of flavin monooxygenases (Mashiguchi et al. 2011, Stepanova et al. 2011, Won et al. 2011) using

NADPH and O2 (Dai et al. 2013).

Regulation of IAA biosynthesis The identification of several auxin biosynthetic genes not only aids with our understanding of how

auxin is made in plants, but also provides new ways to study how the production of this hormone is

regulated with exquisite spatial and temporal resolution. In fact, initial characterization of TAA1/TARs

and several YUC genes in the IPyA pathway unveiled surprisingly specific and dynamic patterns of

expression, suggesting a key role for local auxin biosynthesis in plant development (Stepanova et al.

2008, Tao et al. 2008, Zhao 2010). In addition, the fact that the enzymes catalyzing both steps of the

IPyA pathway are encoded by multigenic families offers a simple mechanism to generate a large

variety of different expression patterns. Thus, for example, tissue/cell-specific auxin biosynthesis can

be accomplished by selectively expressing particular family members in different tissues. This, in fact,

seems to be the case in Arabidopsis, where two separate sets of YUC genes are responsible for auxin

biosynthesis in roots (YUC3, 5, 7, 8, and 9) and in shoots (YUC1, 2, 4, and 6) (Won et al. 2011).

Similarly, the expression of TAA1 and TAR2 genes is also temporally and spatially regulated and

displays extremely specific developmental patterns in embryos, root meristems, and in flowers

(Stepanova et al. 2008, Tao et al. 2008).

The key significance of maintaining specific patterns of auxin production in plant development is

illustrated well by ethylene-mediated root growth inhibition in Arabidopsis. The first piece of evidence

for a connection between ethylene responses and auxin biosynthesis came from the characterization of

mutant alleles of anthranilate synthase genes WEI2/ASA1 and WEI7/ASB1. These mutants display

root-specific ethylene insensitivity due to a defect in an ethylene-triggered auxin biosynthetic surge in

root tips (Stepanova et al. 2005, Ljung et al. 2005). Likewise, roots of taa1 and taa1 tar2 mutants are

resistant to ethylene, again due to the failure to make extra auxin in root tips upon exposure to


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eethylene (Stepanova et al. 2008, Yamada et al. 2009). Transcriptional regulation of these auxin

biosynthetic genes by ethylene was also shown to be important for the positioning of root hairs at the

base of root hair cells (Ikeda et al. 2009), further suggesting that proper levels and distribution of

auxin are a prerequisite for normal plant development. Moreover, the rates of IAA production in roots

were found to be also modulated by cytokinins (Jones et al. 2010), and this effect at least in part is

mediated by the cytokinin-triggered activation of the key auxin biosynthetic gene TAA1 (Zhou et al.

2011). Not surprisingly, some of the root-specific cytokinin responses are impaired in taa1, indicating

that the cytokinin-triggered boost in IAA production is physiologically relevant.

In addition to the aforementioned examples that illustrate regulation of auxin biosynthesis by

plant hormones ethylene and cytokinin, evidences for a role of jasmonate (Dombrecht et al. 2007, Sun

et al. 2009, Hentrich et al. 2013) and ABA (Lee et al. 2012) in the regulation of the production of IAA

are accumulating. Importantly, Hentrich et al. identified YUC8 and 9 as the potential targets of the JA-

mediated control of IAA biosynthesis, pinpointing a possible point of interaction between these two

hormones. Besides plant hormones, environmental factors have also been shown to dramatically affect

the rates of IAA production. For example, plant shading triggers a rapid increase in IAA biosynthesis

(Tao et al. 2008) due to the induction of YUC2, 5, 8 and 9 via PIF7 (Li et al. 2012), resulting in the

enhanced hypocotyl and petiole elongation. Likewise, elevated temperatures have a strong stimulatory

effect on the rates of auxin production (Gray et al. 1998) and several biosynthetic genes, including

TAA1, CYP79B2 and YUC8, were found to be transcriptionally up-regulated by high temperatures in a

PIF4-dependent manner (Franklin et al. 2011, Sun et al. 2012).

The effect of the diurnal fluctuations in the levels of sugars on auxin metabolism represents a

great example of signal integration where auxin biosynthesis plays a central role. The light-dark

cycling levels of carbohydrates correlate well with the rates of IAA production. The auxin biosynthetic

gene YUC9 and the PIF family of transcription factors have been implicated in this signal crosstalk

(Sairanen et al. 2012). The exact molecular mechanisms by which sugar levels regulate growth via

IAA biosynthesis require further investigation, as the genetic analysis of yuc and pif mutants suggests

involvement of a complex regulatory network rather than a direct effect of sugars on PIFs with the

subsequent activation of YUC9 (Lilley et al. 2012, Sairanen et al. 2012). Another connection between

circadian-controlled hypocotyl growth and auxin biosynthesis was established by Rawat et al. (Rawat

et al. 2009) who identified RVE1, a morning-phased transcription factor with homology to the known

core clock components CCA1 and LHY, as a potential integrator of the clock signals and auxin-

mediated hypocotyl growth. Importantly, expression of YUC8 was up-regulated in the RVE1-

overexpressing lines, thus providing a plausible direct mechanistic link between the clock and auxin

biosynthesis.

In addition to the hormonal and environmental regulation, several developmental processes have

also been associated with changes in the IAA biosynthetic activity. Thus, for example, the SHORT-

INTERNODES/STYLISH 1 (SHI/STY1) DNA binding transcription factor has been shown to induce


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eauxin levels and biosynthesis rates in Arabidopsis seedlings via YUC4 (Eklund et al. 2010).

Furthermore, the lack of shoot apical meristems in seedlings carrying a fusion construct between STY1

and a repressor domain, SRDX, suggests that STY1, and probably other SHI/STY members, have a role

in the formation and/or maintenance of the shoot apical meristem, possibly by regulating auxin levels

in the embryo (Eklund et al. 2010). And the list of developmental processes and transcription factors

that affect expression of key auxin biosynthetic genes is quickly expanding. Thus, the NGATHA

family of B3 transcription factors is involved in style development in a dosage-dependent manner, as

shown by the lack of style and stigma tissues in the quadruple ngatha mutant plants. Relevant to this

discussion is the finding that the ngatha mutant phenotypes are in part due to the failure to activate

two YUC genes, YUC2 and 4, in the apical domains of Arabidopsis gynoecia (Trigueros et al. 2009).

Similarly, LEAFY COTYLEDON2 (LEC2), a major regulator of embryogenesis, also induces YUC2

and 4. In fact, LEC2 directly binds to the YUC4 promoter as revealed by ChIP experiments (Stone et

al. 2008). Finally, the PLETHORA (PLT) family of transcription factors has recently been suggested

to play a role in the regulation of local IAA biosynthesis in shoot apexes, where PLT-mediated

regulation of YUC1 and 4 expression was shown to influence phyllotaxis in Arabidopsis (Pinon et al.

2013).

While the examples of auxin biosynthesis modulation via transcriptional changes of key

biosynthetic genes are by far the most abundant in current literature, recent characterization of vas1

mutant, a suppressor of the auxin biosynthetic mutant taa1, unveiled yet another level of interaction

between ethylene and auxin (Zheng et al. 2013). VAS1 is a PLP-dependent aminotransferase that

catalyzes the conversion of IPyA back to Trp, i.e. the reverse reaction of the one catalyzed by TAA1.

Quantification of IPyA and IAA in vas1 and vas1 taa1 mutants revealed accumulation of higher levels

of these compounds than in wild type, indicating that the rescue of IAA biosynthetic defects of taa1 in

the vas1 taa1 doubles is due to the restoration of IPyA pools. In addition, vas1 mutant was able to

rescue many of the severe developmental defects of the taa1 tar2 double mutants, but not that of the

phenotypically similar yuc1 yuc4 mutants. These genetic evidences, together with the IPyA and IAA

quantifications, suggested that VAS1 works downstream of TAA1/TARs but upstream of YUCs,

negatively modulating IAA biosynthesis by altering the availability of IPyA. Consistent with that

hypothesis were the classic low-auxin phenotypes and the reduced IAA content in VAS1ox lines. What

is even more remarkable from the point of view of IAA biosynthesis regulation is that VAS1 represents

a new node of interaction in the well-established crosstalk between auxin biosynthesis and ethylene.

VAS1 uses the ethylene biosynthetic intermediate methionine as an amino donor and the auxin

biosynthetic intermediate IPyA as an amino acceptor to produce Trp and 2-oxo-4-methylthiobutyric

acid. The vas1 mutants thus display concurrently elevated levels of IAA and the ethylene precursor 1-

aminocyclopropane-1-carboxylic acid. Hence, the analysis of VAS1 has unveiled an additional layer of

regulation of auxin biosynthesis that acts at the metabolic level and likely coordinates the biosynthesis

of ethylene and auxin (Zheng et al. 2013).


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eConcluding remarks The identification of several of the key auxin biosynthetic genes in Arabidopsis and the development

of more robust and sensitive analytical methods has brought renewed excitement to the fields of auxin

biosynthesis and auxin-mediated control of plant growth and development. Although the last few years

have witnessed rapid advances in these areas of auxin biology, many unsolved challenges remain. For

example, with the firm establishment of the complete IPyA route of IAA production, the research

focus may now turn towards the investigation of the other proposed biosynthetic pathways, including

the elusive Trp-independent route, shedding light on the thus far undiscovered or poorly characterized

genetic and metabolic components and their regulation, and establishing the relevance of these

pathways to plant growth and development. These efforts should not, however, preclude the

continuing effort to identify the many different developmental and environmental factors that

converge on the transcriptional regulation of the prevalent IPyA route of auxin biosynthesis. We

anticipate that these types of studies will deepen our understanding of the molecular mechanisms of

signal integration in plants in which hormones are known to play a central role. It remains to be seen

how common other types of regulatory mechanisms (beyond traditional transcriptional control) are,

including regulation at the metabolic level, as illustrated above for VAS1, as well as the

posttranscriptional and posttranslational regulation. Perhaps, the ultimate grand challenge of the next

few years would be to elucidate how auxin biosynthesis is integrated in the context of a larger

regulatory network where hormonal, developmental and environmental signals come together to

produce cell-type-specific temporally-controlled developmental and environmental responses.

Acknowledgements – We would like to thank members of the Alonso-Stepanova laboratory and

Kristina Karrass for the critical reading of the manuscript. Work in the Alonso-Stepanova lab is

supported by NSF-MCB0923727 grant to JMA and ANS and NSF-MCB 1158181 grant to JMA. JB

was supported in part by Ministerio de Educacion, Programa Nacional de Movilidad de Recursos

Humanos del Plan Nacional de I-D+i 2008-2011.


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Edited by K. Ljung

Figure legend

Figure 1. Current model of the pathways for indole-3-acetic acid (IAA) biosynthesis in Arabidopsis.

The Tryptophan (Trp) independent route of auxin biosynthesis branches out from the L-Trp

biosynthetic pathway at the level of indole and/or indole-3-glycerol phosphate (IGP). Three Trp-

dependent routes have been proposed: the indole-3-acetaldoxime (IAOx), indole-3-acetamide (IAM),

and the indole-3-pyruvic acid (IPyA). IAN, indole-3-acetonitrile; IGs, indole glucosinolates; CAM,

camalexin. Compounds relevant to IAA synthesis are displayed in black. Solid arrows indicate well-

characterized steps. Dashed arrows mark poorly understood steps or incomplete pathways. Genes

coding for plant enzymes are depicted in blue, while bacterial genes are shown in orange.

Transcription factors that control YUC gene expression are listed in green. Anthranilate synthases

ASA1 (WEI2) and ASB1 (WEI7). Tryptophan aminotransferases (TAA1/TARs). Aminotransferase,

suppressor of TAA1/SAV3 (VAS1). YUCCAs (YUCs). Cytochrome P450 monooxygenases (CYP79B2

and CYP79B3). Indoleacetaldoxime dehydratase (CYP71A13). Nitrilases (NITs). Indole-3-acetamide

hydrolase (AMI1). Myrosinases (MYR). Cytochrome P450 monooxygenases CYP83B1 (SUR2).

Alkylthiohydroximate C-S lyase (SUR1). UDP-glucose:thiohydroximate S-glucosyltransferase

(UGT74B1). Tryptophan monooxygenase (iaaM). Indole-3-acetamide hydrolase (iaaH). Phytochrome

interacting factors (PIFs). Short-internodes/Stylish1 (STY1). NGATHA (NGAs). Leafy cotyledon2

(LEC2). Plethora (PLT).


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e L-Trp

NH

O

OOH

IPyA

NH

N OH

IAOx

IAA

NH

O

NH2

IAMIAN

IGs

Chorismate Anthranilate IGP

IndoleTrp-independentpathw

ay

CAM

PIFsSTY1NGAsLEC2PLT

WEI2WEI7

TAA1TARs

YUCs

CYP79B2CYP79B3

SUR2

SUR1

UGT74B1

CYP71A13

NITs

AMI1/iaaH

? iaaM

MYR

VAS1

NITs


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Genetic aspects of auxin biosynthesis and its regulation