essential roles of local auxin biosynthesis in plant ...biologia.ucr.ac.cr/profesores/garcia...

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Annual Review of Plant Biology

Essential Roles of Local AuxinBiosynthesis in PlantDevelopment and in Adaptationto Environmental ChangesYunde ZhaoSection of Cell and Developmental Biology, University of California, San Diego, La Jolla,California 92093, USA; email: [email protected]

Annu. Rev. Plant Biol. 2018. 69:417–35

First published as a Review in Advance onFebruary 28, 2018

The Annual Review of Plant Biology is online atplant.annualreviews.org

https://doi.org/10.1146/annurev-arplant-042817-040226

Copyright c© 2018 by Annual Reviews.All rights reserved

Keywords

YUCCA, flavin monooxygenase, Arabidopsis, TAA, tryptophan,aminotransferases

Abstract

It has been a dominant dogma in plant biology that the self-organizing polarauxin transport system is necessary and sufficient to generate auxin max-ima and minima that are essential for almost all aspects of plant growthand development. However, in the past few years, it has become clear thatlocal auxin biosynthesis is required for a suite of developmental processes,including embryogenesis, endosperm development, root development, andfloral initiation and patterning. Moreover, it was discovered that local auxinbiosynthesis maintains optimal plant growth in response to environmentalsignals, including light, temperature, pathogens, and toxic metals. In thisarticle, I discuss the recent progress in auxin biosynthesis research and theparadigm shift in recognizing the important roles of local auxin biosynthesisin plant biology.

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ANNUAL REVIEWS Further

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https://www.annualreviews.org/doi/full/10.1146/annurev-arplant-042817-040226


DR5: a highly activesynthetic auxinresponse element

GFP: greenfluorescent protein

GUS:β-glucuronidase

DII-VENUS: theVENUS form ofyellow fluorescentprotein that is fusedin-frame to theAux/IAAauxin-interactiondomain (termeddomain II; DII)

Contents

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 418AN OVERVIEW OF THE CURRENT UNDERSTANDING OF AUXIN

BIOSYNTHESIS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419AUXIN BIOSYNTHESIS IS LOCALIZED AND IS TEMPORALLY

AND SPATIALLY REGULATED . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421LOCAL AUXIN BIOSYNTHESIS IS REQUIRED FOR ALL MAJOR

DEVELOPMENTAL PROCESSES. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423LOCAL DEGRADATION AND INACTIVATION OF AUXIN

ARE IMPORTANT FOR PLANT DEVELOPMENT. . . . . . . . . . . . . . . . . . . . . . . . . . 424PIF-YUC MODULE: REGULATING RESPONSES TO ENVIRONMENTAL

SIGNALS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425Shade Avoidance and Neighbor Detection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425Thermomorphogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427Toxic Metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 428

PLANT-PARASITE AND PLANT-PATHOGEN INTERACTIONSREQUIRE LOCAL AUXIN BIOSYNTHESIS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 428YUC-Mediated Local Auxin Biosynthesis Regulates Haustorium Development . . . . 428Herbivore Attack Rapidly Induces Local Auxin Production for Plant Defense . . . . . . 429

INTRODUCTION

Auxin is an essential hormone for almost every aspect of plant growth and development. One ofthe predominant hypotheses in auxin biology is that auxin is a morphogen and that auxin gradientsdetermine developmental outcomes (4, 30, 39, 42, 55, 91, 103). The effects of exogenous auxintreatments on plant growth and development are concentration dependent: Low concentrationsof exogenous auxin usually promote growth, whereas high concentrations of exogenous auxininhibit growth (19, 58). Petersson et al. (77) observed an auxin gradient and an auxin maximumin the Arabidopsis root apex by using high-resolution cell-specific auxin measurements. Analysesof auxin reporters DR5-GFP/GUS/Luciferase and DII-VENUS in Arabidopsis and other plantspecies also revealed that the expression of the auxin reporters was neither uniform nor ubiquitous(8, 20, 31, 88). Consistently, maxima and minima of the auxin reporter expressions were formedduring embryogenesis, seedling development, and organogenesis, among other developmentalprocesses (1, 5, 6, 32, 38). More importantly, there appears to be a correlation between an auxingradient (defined by DR5 expression) and a particular developmental process. For example, anauxin maximum flanking an apical meristem seems to mark the incipient site of a leaf primordium(1, 47, 92). Furthermore, the auxin maximum at the tip of a lateral organ was proposed as anecessary determinant for primordium outgrowth (30, 55). Whereas peaks of auxin response arewell correlated with organ initiation and outgrowth, auxin minima were proposed to have anessential role in axillary meristem formation and in specification of the valve margin separationlayer in Arabidopsis fruit (24, 85, 105).

Because auxin gradients were proposed to have important roles in plant development, the gen-eration and maintenance of auxin gradients have been studied extensively. The research activitiesin this regard have centered almost exclusively on the analyses of polar auxin transport. It wasobserved that exogenously applied auxin to plant segments moves predominantly from the apical

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PIN1:PIN-FORMED 1

IAA: indole-3-aceticacid

Trp: tryptophan

INS: indole synthase

end to the basal end (shoot to root direction). This directional flow of auxin was termed polar auxintransport, which is achieved through plasma-membrane localized carrier proteins. Early studiesfound that the Arabidopsis pin-formed 1 ( pin1) mutants closely resembled those plants grown onmedia containing the polar auxin transport inhibitor N-1-naphthylphthalamic acid (NPA), sug-gesting that PIN1 plays an important role in auxin transport (34). Moreover, the PIN1 protein waslocated primarily to the basal side of the plasma membrane of parenchymatous xylem cells, con-sistent with the observation that auxin is transported directionally from the apical end to the basalend (34). Therefore, PIN1 and its homologs (PIN proteins) have served as a proxy for studying thedirections and amplitude of polar auxin transport (34, 78, 106). PIN-based mathematical modelswere constructed to predict and explain developmental patterning such as vascular formation,phyllotaxis, lateral organ initiation, and root cell patterning (23, 38, 47, 70, 84, 92). For example,a model based on PIN-mediated transport generated an auxin gradient in a root tip with the auxinmaximum focused at the stem cell niche (38). The model explained the development of sharplybounded meristematic and elongation regions. In this particular model, auxin transport (activetransport and diffusion) alone is sufficient to generate an auxin gradient with an auxin maximum,which is able to guide root growth and the development of different cell types (38). The modeldoes not require local auxin biosynthesis, degradation, or regulated auxin influx for the formationof an auxin maximum (38).

Although the studies of polar auxin transport have been valuable, one caveat is that the sourcesof auxin for a particular transport stream have not been defined. It has generally been assumed thatauxin is ubiquitously produced. Some mathematical models suggest that polar auxin transport is sorobust that the location of auxin production and degradation has little impact on the formation ofauxin gradients (38). However, recent progress in elucidating the molecular mechanisms of auxinbiosynthesis revealed that auxin biosynthesis is surprisingly not ubiquitous; rather, it is localized(13, 15, 16, 33, 79, 95, 99, 121). More importantly, disruption of auxin biosynthesis often causesonly local developmental defects. For example, knockouts of the shoot auxin biosynthetic genescaused dramatic developmental defects in vascular patterning and flower development but feweffects on root development (15). Conversely, disruption of auxin biosynthesis in roots greatlyinhibited primary root elongation and caused agravitropic growth but had little effect on shootgrowth (13). A growing body of literature demonstrates that local auxin biosynthesis is requiredfor all major developmental processes (12, 15, 16, 79, 95, 99, 115). Plants also use local auxinbiosynthesis to optimize their growth when the growth environment undergoes changes (9, 12, 28,61, 69, 72, 76). In this article, I summarize the recent progress in auxin biosynthesis and highlightthe essential roles of local auxin biosynthesis in facilitating various developmental processes andin optimizing growth patterns in response to environmental changes.

AN OVERVIEW OF THE CURRENT UNDERSTANDING OF AUXINBIOSYNTHESIS

Indole-3-acetic acid (IAA), the primary natural auxin, is synthesized from both tryptophan (Trp)-dependent and Trp-independent pathways (7, 49, 51, 119, 120). The Trp-independent pathwaywas initially proposed decades ago on the basis of analyses of the maize Trp auxotrophic mutantorange pericarp (109). A subsequent analysis of Arabidopsis Trp biosynthetic mutants suggested thatthe Trp-independent pathway is used in dicots as well (74). It has been difficult to identify thegenes and intermediates for the Trp-independent pathway. The cytosol-localized indole synthase(INS) is a key enzyme in Trp-independent IAA biosynthesis pathways, and auxin generated fromTrp-independent pathways has an important role in apical–basal pattern formation during earlyembryogenesis in Arabidopsis (104). However, there is a lack of consensus on the exact role of INSin auxin biosynthesis and plant development (73).

www.annualreviews.org • Essential Roles of Local Auxin Biosynthesis 419

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NH

NH

NH

NH

NH

OOH

O

OHO

O

OH

O

OH

O

O

OH

O

OH S

O O

OHNH2

NH2

NH2

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R

OH

TAA YUC DAO

GH3 (VAS2)

VAS1 IAA–amino acid conjugates

MetKMBA

Trp IPA IAA OxIAA

H3CS

H3C

Figure 1The primary auxin biosynthesis and metabolic pathway. IAA, the primary natural auxin, is synthesized fromthe amino acid Trp in two chemical steps. The first step is catalyzed by the TAA family of aminotransferases,which use pyruvate or α-ketoglutarate as an acceptor for the amino group from Trp. The TAA-catalyzedreaction is reversible, and the direction of the reaction is dependent on the availability of the substrates. Thesecond step of IAA biosynthesis is catalyzed by the YUC flavin-containing monooxygenases, which useNADPH and molecular oxygen as co-substrates for the oxidative decarboxylation of IPA. TheYUC-catalyzed reaction is the rate-limiting step in auxin biosynthesis. IAA biosynthesis is tightly regulated.When the IPA level is too high, VAS1, another aminotransferase, converts IPA back to Trp. VAS1 uses theamino acid Met as the amino donor, thus effectively coordinating the biosynthesis of auxin and ethylene. IAAis deactivated through either conjugation to amino acids or chemical oxidation. Conjugation of IAA to aminoacids is catalyzed by GH3-type IAA–amido synthetases. Mutations in VAS2/GH3.17 lead to suppression ofthe shade avoidance defects displayed in taa mutants. IAA can be irreversibly oxidized by DAO, a2-oxoglutarate-dependent-Fe (II) dioxygenase. Coordinated local biosynthesis and degradation ensure localauxin homeostasis, which is required for optimal growth. Abbreviations: DAO, Dioxygenase for AuxinOxidation; GH3, Gretchen Hagen 3; IAA, indole-3-acetic acid; IPA, indole-3-pyruvate; KMBA,α-keto-γ-methiolbutyric acid; Met, methionine; OxIAA, 2-oxoindole-3-acetic acid; SAV, Shade AVoidance;TAA, TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS; Trp, tryptophan; VAS, reversal ofSAV; YUC, YUCCA.

TAA:TRYPTOPHANAMINOTRANS-FERASE OFARABIDOPSIS

YUC: YUCCA

IPA:indole-3-pyruvate

PLP: pyridoxalphosphate

Multiple Trp-dependent auxin biosynthetic routes have been proposed. Several recent reviewshave detailed the evidence (or a lack thereof) supporting the various proposed Trp-dependentauxin biosynthesis pathways (49, 120). So far, only one complete Trp-dependent auxin biosyn-thesis pathway in plants has been firmly established (Figure 1) (21, 67, 96, 107). The TAA/YUC(TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS/YUCCA) pathway convertsTrp to IAA in two consecutive chemical steps (Figure 1). First, Trp is metabolized into indole-3-pyruvate (IPA) by the TAA family of aminotransferases. Second, IPA undergoes oxidative de-carboxylation catalyzed by the YUC family of flavin-containing monooxygenases to produce IAA(Figure 1). In this article, I focus on the TAA/YUC pathway because it is the primary auxinbiosynthesis pathway and because it is required for all major developmental processes.

The role of the TAA/YUC pathway in auxin biosynthesis is well supported by genetic andbiochemical evidence (21, 67, 96, 107). Moreover, the pathway is highly conserved throughoutthe plant kingdom. The pathway has been functionally characterized in Arabidopsis (21, 67, 96,107), rice (Oryza sativa) (48, 108, 111, 115), maize (Zea mays) (33, 79), Brachypodium distachyon(75), petunias (101), liverwort Marchantia (25), and many other species (60, 62). Biochemically,the pathway is not complicated. The first reaction of the pathway uses pyridoxal phosphate (PLP)as a cofactor, and the catalytic mechanism of PLP-dependent transaminases is well understood (95,99). PLP takes the amino group from Trp and transfers it to an α-keto acid. The most commonacceptors of an amino group are pyruvate and α-ketoglutarate. Transaminase-catalyzed reactions

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VAS: reversal of SAV

Met: methionine

are usually reversible and are determined by the availability of substrates. The TAA-catalyzedreaction is generally considered not rate limiting in auxin biosynthesis (95, 99). The second stepof the TAA/YUC pathway requires oxygen and NADPH as co-substrates (Figure 1) (21, 67). Thekey activated intermediate of the YUC-catalyzed reaction is the C4a-hydroperroxyflavin (C4a-FAD), which can take two different routes (21). In the presence of the substrate IPA, the C4aintermediate facilitates the oxidation and decarboxylation of IPA to yield IAA. In the absence ofIPA, the C4a intermediate decays back to the oxidized FAD and releases a molecule of H2O2

(21). Interestingly, approximately 3% of the C4a intermediate decomposes into H2O2 and FADeven if the IPA substrate is present. The intrinsic uncoupling reaction may provide a mechanismfor deactivating YUC flavin-containing monooxygenases (21). Because the C4a intermediate isnot stable and the decomposition product is H2O2, a reactive oxygen species, the YUC proteinsshould be produced only when needed.

The genetic complexity of the TAA/YUC auxin biosynthesis pathway prevented researchersfrom uncovering it for almost a century (15, 95, 99, 121). In this two-step pathway, the enzymesfor each step are encoded by multiple homologous genes. In Arabidopsis, there are at least 4 TAAgenes and 11 YUC genes (15, 95, 99, 121). Knockout of a single TAA or YUC gene in Arabidopsisusually does not cause dramatic developmental phenotypes. Simultaneous disruption of severalTAA or YUC genes causes severe defects in almost all major developmental processes, which canbe rescued by exogenous auxin or by auxin produced in plants with a bacterial auxin biosyntheticgene iaaM (13, 15, 95, 99, 121). Inactivation of TAA genes or YUC genes leads to decreasesin auxin concentrations. Furthermore, the taa mutants contained less IPA, whereas yuc mutantsaccumulated IPA, indicating that TAA aminotransferases are involved in IPA production and thatYUC flavin monooxygenases use IPA as substrate (Figure 1) (67).

Several built-in mechanisms ensure that TAA/YUC-mediated auxin biosynthesis does notget out of control (Figure 1). First, IPA is maintained at a steady concentration. If IPA lev-els are increased, the VAS1 aminotransferase converts IPA back to Trp with Met as the aminodonor (Figure 1) (124). The VAS1-catalyzed reaction effectively couples the biosynthesis of ethy-lene and auxin, two important hormones (124) (Figure 1). Second, the TAA-catalyzed reac-tion is intrinsically reversible and can convert IPA back to Trp if IPA becomes more abundant(Figure 1) (35). The metabolite L-kynurenine, which competes with Trp for the binding sites inTAA aminotransferase, is a widely used auxin biosynthesis inhibitor (41). However, under certainconditions, kynurenine stimulates auxin biosynthesis by preventing TAA from converting IPAback to Trp (35). Third, the availability of YUC flavin monooxygenases is tightly regulated, andthe conversion of IPA to IAA is the rate-liming step in auxin biosynthesis (12, 26, 59, 98, 121).The expression levels of YUC genes correlate with auxin production in plants. Overexpression ofYUC genes in Arabidopsis and rice causes growth and developmental phenotypes (111, 121).

AUXIN BIOSYNTHESIS IS LOCALIZED AND IS TEMPORALLYAND SPATIALLY REGULATED

When the TAA/YUC pathway was elucidated, it was obvious that auxin biosynthesis is not ubiq-uitous. RNA in situ hybridization results showed that an individual YUC gene is expressed only insmall groups of discrete cells (Figure 2a) (15, 16). Analyses of the YUC promoter:GUS transgeniclines also revealed the highly localized patterns of auxin biosynthesis (13). Similarly, TAA genes arenot expressed in all cells, although their expression patterns are broader than those of YUC genes(95, 99). The expression studies revealed that each YUC gene has a distinct expression pattern,and that some YUC genes also have overlapping expression patterns, suggesting that the YUCgenes have overlapping or redundant functions (13, 15, 16). The TAA genes share overlapping


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Shootpromoter YUC3XVE

OP-LexA

Wildtype

yucQ

Mock InductionGrown on MS media

a b

c

yucQ yucQ

The yuc1 yuc4 yuc10 yuc11 quadruple mutants and taa1 tar2 double mutants fail to make the basal part of the embryo. YUC10 and TAR1 are imprinted.

The yuc2 yuc6 double mutants do not produce viable pollen. The yuc1 yuc4 double mutants make fewer floral organs. The yuc1 yuc2 yuc4 yuc6 quadruple mutants produce pin inflorescences. The taa1 tar2 double mutant flowers are sterile.

The yuc1 yuc2 yuc4 yuc6 quadruple mutants do not make tertiary veins. The taa1 tar2 double mutants also make fewer veins.

The yuc3, yuc5, yuc7, yuc8, yuc9 (yucQ) mutant has short and agravitropic roots. Both taa1 and yucQ are resistant to ethylene and the auxin transport inhibitor NPA.

Figure 2Local auxin biosynthesis has essential roles in all major developmental processes. (a) The expression patternof YUC4 in a mature embryo is shown as an example of localized expression of the auxin biosynthetic genes.RNA in situ hybridization results show that YUC4 is expressed only in the apical meristem and at the tip ofcotyledons (black arrows). (b) Mutations in TAA genes or YUC genes result in defects in all majordevelopmental processes. Note that different combinations of yuc mutants affect different developmentalprograms. The mutant phenotypes usually correlate with the expression patterns of the auxin biosyntheticgenes. (c) Auxin required for root development is synthesized mainly in roots, and auxin transported fromshoots is not sufficient to support root development. The yucQ mutants have short and agravitropic roots,which can be rescued by adding low concentrations of auxin to growth media. Auxin can be producedspecifically in shoots by a two-component system. The shoot promoter FRO6p is used to drive the expressionof an artificial transcription factor XVE. In the presence of estradiol, XVE binds to OP-LexA, enablinginductive expression of YUC3. When YUC3 is expressed in shoots, it leads to auxin overproductionphenotypes, including long hypocotyls and epinastic cotyledons, but the root defects in yucQ are not rescued.Abbreviations: MS, Murashige and Skoog; TAA, TRYPTOPHAN AMINOTRANSFERASE OFARABIDOPSIS; XVE, a chimeric transcription activator that is assembled by fusion of the DNA-bindingdomain of the bacterial repressor LexA (X), the acidic trans-activating domain of VP16 (V), and theregulatory region of the human estrogen receptor (E); YUC, YUCCA.

expression patterns as well. Unexpectedly, both TAA and YUC genes are expressed in primary andlateral roots (13, 95, 99). It has long been hypothesized that auxin needed for root developmentoriginates from shoots and is transported downward through the polar auxin transport system (1,38, 100). The emerging picture of auxin biosynthesis is that plants employ a group of YUC andTAA genes to control auxin biosynthesis locally. Precise local auxin production is achieved byexpressing different paralogs of the auxin biosynthetic genes (13, 107).

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LOCAL AUXIN BIOSYNTHESIS IS REQUIRED FOR ALL MAJORDEVELOPMENTAL PROCESSES

Auxin biosynthesis is primarily a localized process, and its impact on plant growth and developmentis largely spatially restricted. Systematic analyses of taa and yuc mutants have demonstrated thatlocal auxin production is required for all major developmental processes (Figure 2b). Local auxinbiosynthesis is required for embryogenesis (16, 95), endosperm development (27), seed develop-ment (3, 18, 52), root development (13, 95, 99), seedling growth (15, 16, 99), vascular patterning(15, 16, 95), phyllotaxis (80), flower development (15, 16, 95), and de novo organogenesis (12, 90)(Figure 2). Overall, the auxin biosynthetic mutant phenotypes correlate well with the expressionpatterns of the auxin biosynthetic genes. For example, YUC1, YUC2, YUC10, and YUC11 arethe primary YUC genes expressed during Arabidopsis embryogenesis (16). The yuc1 yuc4 yuc10yuc11 quadruple mutants fail to develop the basal part of the embryo (Figure 2b) (16). Similarphenotypes are observed in taa1 tar2 double mutants (95). Local auxin biosynthesis has an essen-tial role in vascular formation and patterning, a process that has been studied extensively. Thepredominant hypothesis for vascular patterning is the polar auxin transport–based canalizationtheory (89). In essence, auxin transport–mediated auxin flow determines the number, pattern, andsize of the veins. Auxin biosynthetic yuc1 yuc4 double, yuc1 yuc2 yuc4 triple, and yuc1 yuc2 yuc4 yuc6quadruple mutants produce progressively fewer veins, suggesting that vascular formation requiresa threshold of auxin produced locally by the YUC flavin monooxygenases (15).

Generally, disruption of auxin biosynthetic genes causes developmental defects only in the cellsand tissues in which the auxin biosynthetic genes are expressed. Moreover, the impact of a lack oflocal auxin biosynthesis on the expression of the auxin reporter DR5-GUS/GFP is limited locally.For example, YUC2 and YUC6 are the primary YUC genes expressed during pollen development(10, 11, 15). The yuc2 yuc6 double mutants fail to develop functional mature pollens, but otherdevelopmental processes in the mutants are essentially indistinguishable from those in wild-typeplants (10, 11, 15). DR5 expression is detectable in a developing anther in which the two YUCgenes are expressed. When the two YUC genes are mutated, DR5 expression in the developingpollen disappears as well (11). The correlation of DR5 expression with the expression patternsof YUC genes was also observed during seedling development. YUC1, YUC2, YUC4, and YUC6are the main YUC genes expressed at leaf primordia. DR5 expression was reduced specifically inthe emerging leaflets in the yuc1 yuc4 double mutants. Such a local reduction of DR5 expressioncorrelates with the findings that the YUC genes mark the incipient sites of leaf development andthat they are expressed in young leaves (16, 118).

Temporally and spatially regulated auxin biosynthesis controls Arabidopsis endosperm devel-opment (27). Before fertilization, the central cell does not divide because the expression of theauxin biosynthetic genes YUC10 and TAR1 is epigenetically blocked by the Polycomb group pro-tein family (Figure 2b). Fertilization removes the epigenetic suppression and induces local auxinbiosynthesis in the central cell. The newly synthesized auxin triggers central cell division and pro-liferation. Production of auxin in the central cell is necessary for proper endosperm developmentand is sufficient to trigger central cell division (27). In the early stages of endosperm development,locally produced auxin (not auxin transported from other cells or tissues) directs proper cell divi-sion events (27). YUC-mediated auxin biosynthesis is also required for endosperm developmentin maize (3).

The essential roles of auxin in root development are well established, but investigators havegiven conflicting accounts for the origin of auxin required for root development. Polar auxintransport is necessary for proper root development. For example, both aux1 and pin2, whichencode an auxin influx carrier and an auxin efflux carrier, respectively, do not properly respond togravity stimuli (2, 14, 64). Therefore, it was hypothesized that auxin required for root development


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ACC:1-aminocyclopropane-1-carboxylic acid

NPA: N-1-naphthylphthalamicacid

GH3: GretchenHagen 3

is first synthesized in shoots and then transported downward through the central vascular tissuesto the root tip (38). Then auxin is transported upward from the root tip through epidermal cells.The so-called fountain model of auxin transport has been used to account for root elongation androot gravitropic responses (100). Research conducted over the past few years has elucidated thatauxin biosynthetic genes are expressed in roots and that auxin is synthesized in roots. The essentialroles of local auxin biosynthesis in root development were revealed when the auxin biosyntheticmutants showed dramatic defects in roots (Figure 2b). Mutations in the TAA1 gene altered the rootresponse to gravity, 1-aminocyclopropane-1-carboxylic acid (ACC), and N-1-naphthylphthalamicacid (NPA), and the phenotypes are caused by a reduction of auxin in roots (95, 99, 110). BecauseTAA1 is expressed in the shoot as well, it was difficult to determine whether the reduction of auxinconcentration is caused by reduced auxin synthesis in roots, reduced transport from the shoot, orboth.

The YUC3, YUC5, YUC7, YUC8, and YUC9 genes are expressed in roots, and inactivation ofthese five YUC genes ( yucQ) leads to the development of short and agravitropic roots (Figure 2c).To determine the relative contributions of local auxin biosynthesis in roots and of polar auxintransport from shoots to roots, Chen et al. (13) used an inducible expression system to specificallyoverexpress a YUC gene in shoots in a yucQ mutant background. Whereas expression of a YUC genein roots completely rescued the short root and agravitropic phenotypes of yucQ, overexpressionof a YUC gene in shoots failed to rescue the root defects of yucQ (Figure 2c). Despite the obviousauxin overproduction phenotypes in shoots caused by overexpression of the YUC gene (Figure 2c),yucQ roots were still short and did not properly respond to gravity, demonstrating that auxinproduced in shoots is not sufficient to support root development (13).

LOCAL DEGRADATION AND INACTIVATION OF AUXINARE IMPORTANT FOR PLANT DEVELOPMENT

Conjugation of IAA to amino acids catalyzed by the Gretchen Hagen 3 (GH3) family of IAA–amido synthetases has an important role in regulating local concentrations of auxin (Figure 1)(40, 94). Zheng et al. (123, 124) conducted a genetic screen for second site mutations that cansuppress the shade avoidance defects of taa1/sav3, which encodes a TAA aminotransferase forauxin biosynthesis (Figure 1). The taa1/sav3 mutants fail to elongate their hypocotyls in responseto shade conditions (99). Two interesting suppressors, vas1 and vas2 (vas stands for the rever-sal of sav), were isolated from the genetic screen. VAS1 is an aminotransferase that specificallyuses IPA and Met as the acceptor and donor, respectively, of the amino group (Figure 1) (124).VAS2 is the IAA–amido synthetase GH3.17, which catalyzes the conjugation of free IAA to Glu(Figure 1). IAA-Glu is considered inactive and destined to eventual degradation because exoge-nously applied IAA-Glu does not cause auxin over-accumulation phenotypes, and no amidohydro-lase has been identified as responsible for the release of free IAA from the conjugate. Mutations inVAS2/GH3.17 lead to an increase of free IAA and a decrease of IAA-Glu (123). Consequently, vas2has long hypocotyls when grown in both normal and shade conditions. VAS2/GH3.17 is expressedpredominantly in hypocotyls and its expression in hypocotyls is regulated by light conditions.Shade treatments significantly downregulate VAS2 expression in the hypocotyl, which ensuresthat free IAA rapidly accumulates in hypocotyls to stimulate hypocotyl elongation. VAS2/GH3.17functions locally, which is also supported by the observation that vas2 functions independently ofpolar auxin transport (123). The auxin transport inhibitor NPA can fully inhibit shade-inducedhypocotyl elongation in Arabidopsis, presumably because free IAA in cotyledons is prevented frombeing transported to hypocotyls. However, under the same conditions, shade-stimulated hypocotylelongation of vas2 mutants and vas2 sav3 double mutants was hardly affected by NPA. The vas2

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OxIAA:2-oxoindole-3-aceticacid

DAO: Dioxygenasefor Auxin Oxidation

mutant has longer hypocotyls under shade conditions even when polar auxin transport from cotyle-dons to hypocotyls is inhibited. Another interesting observation is that hypocotyl elongation invas1 sav3 double mutants is fully inhibited by NPA. The observed difference in how vas1 andvas2 respond to treatments with NPA suggests that the accumulation of free IAA in vas2 mutanthypocotyls occurs independently of newly synthesized auxin in cotyledons (123).

VAS2 belongs to the GH3 family, which has eight IAA–amido synthetases in Arabidopsis. In-terestingly, among the GH3 family members, only VAS2/GH3.17 and GH3.9, which is the closestparalog of VAS2, are not rapidly induced by exogenous auxin treatments. Induction of GH3 ex-pression by IAA provides an effective means to prevent over-accumulation of free IAA. Althoughboth VAS2 and GH3.9 can conjugate IAA to Glu in vitro, disruption of GH3.9 cannot suppresstaa1/sav3, indicating that VAS2 and GH3.9 are not redundant in vivo. The phenotypic differencebetween vas2 and gh3.9 could be caused by the differences in their expression patterns. GH3.9 isexpressed predominantly in siliques. Local activation of VAS2/GH3.17 effectively modulates auxinmetabolism and rapid auxin spatial redistribution in response to environmental changes (123).

Recent findings demonstrated that auxin degradation has critical roles in maintaining localauxin homeostasis and normal plant development. IAA is oxidized into 2-oxoindole-3-acetic acid(OxIAA) in plants, the first step toward the complete degradation of IAA (Figure 1). Conversionof IAA to OxIAA is catalyzed by DAO (Dioxygenase for Auxin Oxidation), a 2-oxoglutarate-dependent-Fe (II) dioxygenase (122). DAO was first characterized in rice and then subsequentlystudied in Arabidopsis. In rice, mutations in the DAO gene lead to the development of partheno-carpic seeds filled with a sucrose-rich liquid. The dao flowers do not open and do not release anyviable pollens (122). The dao mutants contain no detectable OxIAA in flowers and leaves, indicat-ing that DAO is the primary enzyme that oxidizes IAA into OxIAA in rice (122). Consistent withthe hypothesis that DAO converts free IAA to OxIAA, the dao mutants contain elevated concen-trations of free IAA and show increased DR5-GUS expression (122). Moreover, the formation ofparthenocarpic seeds is phenocopied by overexpressing a YUC gene in wild-type plants or by ap-plying exogenous auxin to wild-type plants (122). DAO is expressed in roots, stems, leaves, lemma,and palea, but it is expressed predominantly in the mature anther and fertilized ovary (122). DAOprotein is also detected primarily in the extracts of wild-type anthers (122). The observable phe-notypes in dao mutants correlate well with the expression patterns of DAO, suggesting that localdegradation of auxin has important roles in plant development (122). In Arabidopsis, disruptionof AtDAO1 resulted in only subtle phenotypes in shoot and root development (68, 81, 116, 117).Metabolic profiling showed that OxIAA concentrations in Atdao mutants decreased 50%, whereasthe mutations increased IAA-Glu and IAA-Asp 438-fold and 240-fold, respectively, suggestingthat auxin oxidation and conjugation are redundantly used to maintain local auxin homeostasis inArabidopsis (68, 81, 116).

PIF-YUC MODULE: REGULATING RESPONSES TO ENVIRONMENTALSIGNALS

Shade Avoidance and Neighbor Detection

When plants are grown under shade or foliar canopy, they undergo a series of growth and devel-opmental changes, including elongation of hypocotyls, stems, and petioles and development ofhyponastic leaves (9, 28, 43). The so-called shade avoidance syndrome (SAS) provides an adaptiveadvantage by enabling plants to grow quickly to reach light. A related process called neigh-bor detection allows plants to detect their competitors and to anticipate potentially unfavorablelight conditions even before the actual shade conditions are developed. Both SAS and neighbor


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Elev

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Time

IAA at the tip

Mock

White light

PIFsShade or hightemperature

Other signals

Phytochromes YUCs Auxin Adaptive responses

a

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c

White light supplemented with FR to the whole plant

White light with spotted FR at the tip of a leaf (red spot)

Figure 3Important roles of local auxin biosynthesis mediated by the PIF-YUC module in adaptation toenvironmental changes. (a) The PIF-YUC module. PIF transcription factors interact with phytochromes.When in shade, phytochrome B is converted to the inactive Pr form, and PIF transcription factors arereleased to activate YUC transcription, resulting in localized auxin biosynthesis. (b) Localized shade-inducedauxin biosynthesis mediated by PIF-dependent expression of the YUC genes is both necessary and sufficientto trigger leaf hyponasty. Local expression of a YUC gene at a leaf tip or application of exogenous auxin atthe leaf tip (red spots) is sufficient to elevate the leaf angle (red trace). More importantly, the hyponasticresponse is restricted to the treated leaf only, demonstrating that local auxin biosynthesis triggers a localresponse. (c) Spot irradiation with FR is sufficient to trigger leaf hyponasty. Supplemental FR treatment tothe whole plant simulates shade conditions and triggers petiole elongation and leaf hyponasty (middle plant).Spot irradiation with FR (red spot) at the leaf tip also triggers leaf hyponasty, but the response is restricted tothe treated leaf only (right plant). Moreover, spot irradiation does not cause petiole elongation. FRtreatments convert phytochrome B to the inactive Pr form and release PIF transcription factors that activateYUC-mediated local auxin biosynthesis. Abbreviations: FR, far-red light; IAA, indole-3-acetic acid; PIF,phytochrome-interacting factor; Pr, red light–absorbing form of phytochrome; YUC, YUCCA.

FR: far-red light

PIF: phytochrome-interacting factor

Pfr: far-redlight–absorbing formof phytochrome

Pr: redlight–absorbing formof phytochrome

detection rely on the perception of the red (R)-to-far-red (FR) ratio (R:FR ratio) by phytochromes(9, 28). De novo auxin biosynthesis is required for SAS, as both taa mutants and yuc mutants are in-sensitive to shade conditions (50, 71, 99, 107). Recent studies have established a signaling pathwaybeginning where changes to the R:FR ratio are detected, which triggers extensive transcriptionreprogramming mediated primarily by the PIF (phytochrome-interacting factor) family of basichelix–loop–helix transcription factors (Figure 3a) (44, 57). Three PIF transcription factors, PIF4,PIF5, and PIF7, function downstream of the phytochromes during SAS and neighbor detectionto regulate auxin biosynthesis by binding directly to promoters of YUC genes (44, 57, 69). Un-der normal light conditions, phytochrome B (phyB) stays in the active Pfr form and binds toPIF transcription factors, causing PIF transcription factors to become phosphorylated and de-graded. Under shade conditions, phyB stays in the inactive Pr form (the red light–absorbing formof phytochrome), and consequently PIF transcription factors remain free and can activate auxinbiosynthesis (Figure 3a).

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Shade induces quick auxin production in cotyledons by the TAA/YUC pathway, and the newlyproduced auxin is then transported to the hypocotyl to induce its elongation. However, localauxin biosynthesis is necessary and sufficient to trigger leaf hyponasty in response to simulatedshade conditions (Figure 3b) (69, 76). Moreover, local induction of auxin synthesis in one leafleads to a hyponastic response in only that particular leaf and does not affect the developmentof other leaves on the same plant (Figure 3b) (69, 76). Michaud et al. (69) manipulated localconcentrations of auxin in Arabidopsis leaves by local application of exogenous auxin and by localauxin biosynthesis mediated by YUC gene expression. They discovered that applying auxin orinducing YUC expression at the leaf tip phenocopies the hyponastic response induced by a lowR:FR ratio (simulated shade). In contrast, applications of auxin or expressing the YUC genes atpetioles did not elicit the hyponastic response, indicating that where auxin is produced has aprofound impact on how plants respond to changes in light conditions (69).

In a complementary study, Pantazopoulou et al. (76) applied a 3.5-mm-diameter spotlight ofFR irradiation to different regions of an Arabidopsis leaf (Figure 3c). Such a treatment lowers thelocal R:FR ratio, converts phyB to the inactive Pr form locally, and leads PIF transcription factorsto accumulate at the spot (Figure 3a) (76). When an entire leaf is irradiated with FR (FRwhole),leaf hyponasty is observed as expected (76). Leaf hyponasty is also achieved when only the leaftip is treated with FR (FRtip). In contrast, spot irradiation with FR at petioles does not causeleaf hyponasty (76). Interestingly, leaf hyponasty by FRtip appears to be even more pronounced.Moreover, FRwhole-induced leaf hyponasty can be completely reversed by applying R irradiation atthe leaf tip, further supporting the finding that lowering the R:FR ratio at the leaf tip is necessaryand sufficient to induce leaf hyponasty (76). Pantazopoulou et al. (76) also noticed that productionof auxin in one leaf mediated by changing the local R:FR ratio does not trigger an auxin responsein other rosette leaves, indicating that auxin synthesis is local and the response is also restrictedlocally.

Unlike leaf hyponasty induced by producing auxin at the leaf tip or by lowering the R:FRratio at the tip, petiole elongation is stimulated by FR treatment of the whole plant (FRwhole),whereas FRtip does not affect petiole elongation (76). Spot irradiation with FR at different regionschanges the R:FR ratio and causes local auxin production mediated by PIF-dependent YUC geneexpression (Figure 3a). In this process, PIF7 appears to have a predominant role. The pif7 mutantlacks any hyponastic response to either FRwhole or FRtip. The expression of both YUC8 and YUC9in the lamina tip is also abolished in the pif7 mutant (76). The PIF7-YUC module in the leaf tipdetermines local auxin biosynthesis and responses to shade conditions.

Phototropism enables plants to grow toward a light source, and phototropins are the bluelight receptors responsible for detecting directional light. The phototropic response is enhancedunder shade conditions (36). The promotion of phototropism by shade is dependent on local auxinproduction mediated by the PIF-YUC module. Overexpression of PIF promotes phototropism,as does local induction of YUC gene expression (36). Moreover, induction of YUC3 in pif4 pif5pif7 triple mutants rescued the inhibition of phototropism, demonstrating that regulated YUCexpression by PIF transcription factors is a key regulatory step in phototropism (36).

Thermomorphogenesis

Thermomorphogenesis refers to a suite of morphological and architectural changes induced byelevated ambient temperatures (87). Developmental changes induced by high ambient tempera-tures are in many ways similar to those stimulated by shade (86). For example, both shade andhigh temperature stimulate the elongation of hypocotyls and petioles (37, 86). It is not surpris-ing that shade avoidance and thermomorphogenesis may share similar molecular mechanisms.


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PIF4, PIF3, and, to some degree, PIF5 have emerged as the regulatory hub of thermomorpho-genesis, and pif4 mutants fail to elongate their hypocotyls at high ambient temperatures (29, 82,83, 86). PIF4 is regulated transcriptionally and post-transcriptionally and by epigenetic modifi-cations (17, 22, 46, 53, 102). Despite the complexity of PIF4 functions in thermomorphogenesis,the PIF-YUC module has a critical role in high-temperature-mediated hypocotyl elongation.High-temperature-induced hypocotyl elongation in Arabidopsis is caused by elevated concentra-tions of auxin (37). Several auxin biosynthetic genes, including TAA1, YUC8, and CYP79B2, aredirect targets of PIF4 (29, 97). PIF4 interacts with phyB, which was recently proposed as a planttemperature sensor (54, 93). Warm temperatures reduce the abundance of the active phyB pool,thus freeing PIF4 to activate auxin biosynthesis. PIF4 also interacts with the blue light receptorCRY1 in a blue light–dependent manner (65). One consequence of the PIF4-CRY1 interactionis the inhibition of PIF4’s transcription activity, which partially explains why blue light inhibitshypocotyl elongation under both 22◦C and 29◦C. YUC8 was upregulated in cry1 mutants, andCRY1 decreased PIF4-mediated YUC expression in a transient assay (65). The flowering timecontrol protein FCA, which is also an RNA-binding protein, interacts with PIF4 and attenuatesPIF4 activities, thus preventing YUC8 from being induced at high temperature (53).

Toxic Metals

Toxic metals inhibit plant growth. For example, aluminum (Al) ions greatly inhibit root elongationin Arabidopsis (113). Al toxicity is dependent partially on auxin (59, 112). The auxin biosyntheticmutant taa1 was less sensitive to Al than wild-type plants were, and the addition of auxin to growthmedia enhances the inhibitory effects of Al on root elongation (112). YUC flavin monooxygenasesare also required for the full toxicity of Al on root growth. Interestingly, the expression of severalYUC genes, including YUC3, YUC5, YUC7, YUC8, and YUC9 (the root YUC genes), is inducedwhen roots are treated with Al (59). PIF4 also appears to have a role in response to Al-inducedstress. Disrupting PIF4 expression significantly alleviates the inhibition of root growth caused byAl-induced stress, whereas overexpression of PIF4 strengthened the inhibitory effects of Al. PIF4binds directly to the promoters of YUC5, YUC8, and YUC9 to promote local auxin biosynthesisin the root-apex transition zone when plants face Al-induced stress, thus demonstrating anotherexample of the important roles of the PIF-YUC module (Figure 3a) (59).

PLANT-PARASITE AND PLANT-PATHOGEN INTERACTIONSREQUIRE LOCAL AUXIN BIOSYNTHESIS

YUC-Mediated Local Auxin Biosynthesis Regulates Haustorium Development

A recent study of parasitic plant–host plant interactions demonstrates the importance of localauxin biosynthesis (Figure 4) (45). Parasitic plants can devastate agricultural productivity whenthey infect economically important crops such as corn. A key step during infection of a hostplant by a parasitic plant is the formation of a haustorium, a multicellular organ that penetratesthe host tissues (Figure 4) (45). Host-derived chemicals such as 2,6-dimethoxy-p-benzoquinone(DMBQ) can activate haustoria formation in parasitic roots in the absence of a host plant. Ishidaet al. (45) used the facultative parasitic plant Phtheirospermum japonicum to study the molecularmechanisms by which haustoria formation is initiated. They identified and analyzed the P. japon-icum genes induced by DMBQ. The gene Pj-YUC3 clustered with the Arabidopsis YUC3, YUC5,YUC7, YUC8, and YUC9, which are the root YUC genes. Pj-YUC3 was highly upregulated oneday after treatment with host root exudate and was induced by more than 200-fold two days

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YUYUC3C3YUC3

a b

Parasiticplant root

Hostplant root

Figure 4Development of haustoria in the parasitic plant Phtheirospermum japonicum is controlled by YUC-mediatedlocal auxin biosynthesis. (a) A haustorium is formed when the parasitic plant P. japonicum infects anArabidopsis root. The vascular tissues in both host and parasitic plants are stained in red. Panel a was kindlyprovided by Dr. Ken Shirasu at RIKEN Japan. (b) Expression of YUC3 is necessary and sufficient to inducethe formation of a haustorium. During an infection, YUC3 is expressed primarily within the epidermal andouter cortical layers of the region where haustorium growth is initiated ( green dots), which is located at theinterface between the host and parasitic roots.

after treatment. Upregulation of Pj-YUC3 was also observed in haustorial tissues post infection.More importantly, the expression of Pj-YUC3 is highly localized (Figure 4) (45). Its expressionlocalizes to the haustorium apex and haustorial hairs. Spatially, Pj-YUC3 was expressed primarilyat the interface between the host and the parasitic root (45). The induction of Pj-YUC3 expres-sion also correlates with an increase in auxin concentration following root exudate treatment.Expression of DR5 correlates with the patterns of Pj-YUC3 expression during the early stages ofhaustorium development. Genetic studies demonstrated that local expression of Pj-YUC3 andlocal auxin biosynthesis are necessary and sufficient to induce a haustorium-like structure inP. japonicum roots (45). Knockout of YUC3 in P. japonicum roots significantly decreases the fre-quency of haustoria formation. On the other hand, ectopic expression of Pj-YUC3 at the rootepidermal cells stimulates haustorium-like structures to form in the absence of a host or withouthost root exudate treatment. The early stages of haustorium development appear to be controlledprimarily by YUC-mediated local auxin biosynthesis, and the involvement of polar auxin transportis minimal (45).

Herbivore Attack Rapidly Induces Local Auxin Production for Plant Defense

Jasmonates ( JAs) are recognized as the prominent hormone in plant defense against herbivores (56,63, 114). However, a recent study has revealed that auxin may also have a key role in this process(66). Using the herbivore Manduca sexta (tobacco hornworm) and its host plant Nicotiana attenuata,


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Machado et al. (66) discovered that herbivore attack or simulated herbivore attack (treatments withherbivore oral secretions and fatty acid conjugate elicitors) induces auxin to rapidly accumulateat the site of attack. The accumulation of IAA is so fast that it precedes the JA burst, a defensiveresponse by plants against herbivores. Moreover, the accumulation of IAA does not require JAsignaling (66). N. attenuata has at least nine YUC-like genes. Upon application of M. sexta oralsecretions and fatty acid conjugates to the host plant, the expression of NaYUCCA-like 1, 3, 5, 6,and 9 genes is induced within 3 minutes. The induction of the YUC genes is likely responsiblefor the rapid accumulation of IAA upon herbivore attack (66), suggesting that de novo auxinbiosynthesis has a critical role in plant defense against this herbivore.

SUMMARY POINTS

1. Auxin is produced in plants primarily by the two-step Trp-dependent auxin biosynthesispathway catalyzed by the TAA family of transaminases and the YUC family of flavinmonooxygenases. The pathway is conserved throughout the plant kingdom.

2. Both TAA genes and YUC genes are not expressed ubiquitously. Rather, their expressionis localized. Where auxin is produced in the plant has a profound impact on plant growthand development.

3. Auxin required for root development is synthesized mainly in roots by the TAA/YUCpathway, and shoot-derived auxin is not sufficient to support root growth in Arabidopsis.

4. Local auxin biosynthesis is necessary and sufficient for several developmental processes,including endosperm development, leaf hyponasty under shade conditions, and somehost–parasite interactions.

DISCLOSURE STATEMENT

The author is not aware of any affiliations, financial holdings, funding, or memberships that maybe perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

I thank Dr. Ken Shirasu for providing the image of haustorium development. I also thank Drs.Hongtao Liu, Youfa Cheng, and Yun Hu for comments and Yi-Dong Wang for assistance withthe artwork for the figures. My research is supported by NIH grant R01GM114660.

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PP69_FrontMatter ARI 5 April 2018 9:11

Annual Review ofPlant Biology

Volume 69, 2018

Contents

My Secret LifeMary-Dell Chilton � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Diversity of Chlorophototrophic Bacteria Revealed in the Omics EraVera Thiel, Marcus Tank, and Donald A. Bryant � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �21

Genomics-Informed Insights into Endosymbiotic Organelle Evolutionin Photosynthetic EukaryotesEva C.M. Nowack and Andreas P.M. Weber � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �51

Nitrate Transport, Signaling, and Use EfficiencyYa-Yun Wang, Yu-Hsuan Cheng, Kuo-En Chen, and Yi-Fang Tsay � � � � � � � � � � � � � � � � � � � � �85

Plant VacuolesTomoo Shimada, Junpei Takagi, Takuji Ichino, Makoto Shirakawa,

and Ikuko Hara-Nishimura � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 123

Protein Quality Control in the Endoplasmic Reticulum of PlantsRichard Strasser � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 147

Autophagy: The Master of Bulk and Selective RecyclingRichard S. Marshall and Richard D. Vierstra � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 173

Reactive Oxygen Species in Plant SignalingCezary Waszczak, Melanie Carmody, and Jaakko Kangasjarvi � � � � � � � � � � � � � � � � � � � � � � � � � � 209

Cell and Developmental Biology of Plant Mitogen-Activated ProteinKinasesGeorge Komis, Olga Samajova, Miroslav Ovecka, and Jozef Samaj � � � � � � � � � � � � � � � � � � � � � 237

Receptor-Like Cytoplasmic Kinases: Central Players in Plant ReceptorKinase–Mediated SignalingXiangxiu Liang and Jian-Min Zhou � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity toImmunity and BeyondChristina Maria Franck, Jens Westermann, and Aurelien Boisson-Dernier � � � � � � � � � � � � 301

Kinesins and Myosins: Molecular Motors that Coordinate CellularFunctions in PlantsAndreas Nebenfuhr and Ram Dixit � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 329

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The Oxylipin Pathways: Biochemistry and FunctionClaus Wasternack and Ivo Feussner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 363

Modularity in Jasmonate Signaling for Multistress ResilienceGregg A. Howe, Ian T. Major, and Abraham J. Koo � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 387

Essential Roles of Local Auxin Biosynthesis in Plant Developmentand in Adaptation to Environmental ChangesYunde Zhao � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 417

Genetic Regulation of Shoot ArchitectureBing Wang, Steven M. Smith, and Jiayang Li � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 437

Heterogeneity and Robustness in Plant Morphogenesis: From Cellsto OrgansLilan Hong, Mathilde Dumond, Mingyuan Zhu, Satoru Tsugawa,

Chun-Biu Li, Arezki Boudaoud, Olivier Hamant, and Adrienne H.K. Roeder � � � � � � 469

Genetically Encoded Biosensors in Plants: Pathways to DiscoveryAnkit Walia, Rainer Waadt, and Alexander M. Jones � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 497

Exploring the Spatiotemporal Organization of Membrane Proteins inLiving Plant CellsLi Wang, Yiqun Xue, Jingjing Xing, Kai Song, and Jinxing Lin � � � � � � � � � � � � � � � � � � � � � � � 525

One Hundred Ways to Invent the Sexes: Theoretical and ObservedPaths to Dioecy in PlantsIsabelle M. Henry, Takashi Akagi, Ryutaro Tao, and Luca Comai � � � � � � � � � � � � � � � � � � � � � � 553

Meiotic Recombination: Mixing It Up in PlantsYingxiang Wang and Gregory P. Copenhaver � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 577

Population Genomics of Herbicide Resistance: Adaptation viaEvolutionary RescueJulia M. Kreiner, John R. Stinchcombe, and Stephen I. Wright � � � � � � � � � � � � � � � � � � � � � � � � � 611

Strategies for Enhanced Crop Resistance to Insect PestsAngela E. Douglas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 637

Preadaptation and Naturalization of Nonnative Species: Darwin’s TwoFundamental Insights into Species InvasionMarc W. Cadotte, Sara E. Campbell, Shao-peng Li, Darwin S. Sodhi,

and Nicholas E. Mandrak � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 661

Macroevolutionary Patterns of Flowering Plant Speciationand ExtinctionJana C. Vamosi, Susana Magallon, Itay Mayrose, Sarah P. Otto,

and Herve Sauquet � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 685

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When Two Rights Make a Wrong: The Evolutionary Genetics ofPlant Hybrid IncompatibilitiesLila Fishman and Andrea L. Sweigart � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 707

The Physiological Basis of Drought Tolerance in Crop Plants:A Scenario-Dependent Probabilistic ApproachFrancois Tardieu, Thierry Simonneau, and Bertrand Muller � � � � � � � � � � � � � � � � � � � � � � � � � � � � 733

Paleobotany and Global Change: Important Lessons for Species toBiomes from Vegetation Responses to Past Global ChangeJennifer C. McElwain � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 761

Trends in Global Agricultural Land Use: Implications forEnvironmental Health and Food SecurityNavin Ramankutty, Zia Mehrabi, Katharina Waha, Larissa Jarvis,

Claire Kremen, Mario Herrero, and Loren H. Rieseberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 789

Errata

An online log of corrections to Annual Review of Plant Biology articles may be found athttp://www.annualreviews.org/errata/arplant

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essential roles of local auxin biosynthesis in plant ...biologia.ucr.ac.cr/profesores/garcia...

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