Auxin EvoDevo: Conservation and Diversification of Genes Regulating Auxin Biosynthesis, Transport, and Signaling

Molecular Plant Review Article

Auxin EvoDevo: Conservation and Diversification of Genes Regulating Auxin Biosynthesis, Transport, and Signaling Michaela Sylvia Matthes1,6, Norman Bradley Best1,6, Janlo M. Robil1, Simon Malcomber2,5, Andrea Gallavotti3,4 and Paula McSteen1,* 1

Division of Biological Sciences, Interdisciplinary Plant Group and Missouri Maize Center, University of Missouri–Columbia, 301 Christopher Bond Life Sciences Center, Columbia, MO 65211, USA

2

Department of Biological Sciences, California State University, Long Beach, CA 90840, USA

3

Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ 08854-8020, USA

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Department of Plant Biology, Rutgers University, New Brunswick, NJ 08901, USA

5Present 6These

address: National Science Foundation, 2415 Eisenhower Avenue, Alexandria, VA 22314, USA

authors contributed equally to this article.

*Correspondence: Paula McSteen ([email protected]) https://doi.org/10.1016/j.molp.2018.12.012

ABSTRACT The phytohormone auxin has been shown to be of pivotal importance in growth and development of land plants. The underlying molecular players involved in auxin biosynthesis, transport, and signaling are quite well understood in Arabidopsis. However, functional characterizations of auxin-related genes in economically important crops, specifically maize and rice, are still limited. In this article, we comprehensively review recent functional studies on auxin-related genes in both maize and rice, compared with what is known in Arabidopsis, and highlight conservation and diversification of their functions. Our analysis is illustrated by phylogenetic analysis and publicly available gene expression data for each gene family, which will aid in the identification of auxin-related genes for future research. Current challenges and future directions for auxin research in maize and rice are discussed. Developments in gene editing techniques provide powerful tools for overcoming the issue of redundancy in these gene families and will undoubtedly advance auxin research in crops. Keywords: auxin, maize, Arabidopsis, rice Matthes M.S., Best N.B., Robil J.M., Malcomber S., Gallavotti A., and McSteen P. (2019). Auxin EvoDevo: Conservation and Diversification of Genes Regulating Auxin Biosynthesis, Transport, and Signaling. Mol. Plant. 12, 298–320.

INTRODUCTION The focus of this review is to highlight the conservation and diversification of auxin-related gene family members in representative monocot (Zea mays [maize] and Oryza sativa [rice]) versus eudicot (Arabidopsis thaliana [Arabidopsis]) species and to provide insights for future directions of auxin research. The origins of the genes controlling auxin biosynthesis, transport, and signaling in the evolutionary history of plants is an active area of research and has been reviewed recently (Finet and Jaillais, 2012; Kato et al., 2018; Thelander et al., 2018). Auxin is an ancient molecule that is produced from tryptophan (Trp) in plants, algae, and bacteria (Cooke et al., 2002) and has similarities in structure with melatonin in animals (Arnao and Herna´ndez-Ruiz, 2017). Auxin biosynthetic enzymes are predicted to have been present in the common ancestor of land plants and charophyte 298

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algae (streptophytes) 850 million years ago (mya) (Poulet and Kriechbaumer, 2017; Romani, 2017). Charophyte algae and the bryophyte Physcomitrella patens also exhibit polar auxin transport (PAT) (Boot et al., 2012; Bennett et al., 2014; Viaene et al., 2014), indicating that PAT already existed prior to the transition of plants onto land. However, a fully functioning nuclear auxin signaling pathway evolved much later, approximately 530 mya, and is first detected in the earliest diverging land plants, the bryophytes (moss, liverworts, and hornworts) (Mutte et al., 2018). Research on the bryophytes P. patens and Marchantia polymorpha and the lycophyte Selaginella moellendorffii provides essential information on ancient functions of auxin without the

Published by the Molecular Plant Shanghai Editorial Office in association with Cell Press, an imprint of Elsevier Inc., on behalf of CSPB and IPPE, SIBS, CAS.

Auxin EvoDevo Review complexity of gene families seen in angiosperms (Kato et al., 2018; Thelander et al., 2018). Gene families controlling auxin biosynthesis, transport, and signaling have greatly expanded and diversified in eudicots and monocots in the last 150 million years, highlighting the need for functional analysis in higher plant species, especially in crops. To examine the conservation and diversification of the gene families controlling auxin biosynthesis, transport, and signaling in monocots and eudicots, we highlight functional analyses in maize and rice, and compare them with Arabidopsis. As the nomenclature for mutants and genes is not consistent across species, we provide a summary table of the functionally characterized auxin family members discussed (Supplemental Table 1). Comparing and contrasting function in monocots and eudicots also requires knowledge of orthologs, co-orthologs, and paralogs, and how expression patterns are conserved or differ and show evidence of sub-functionalization. Therefore, we illustrate our points by combining phylogenetic analysis of auxin biosynthesis, transport, and signaling gene families (Figures 1, 2, 3, 4, 5, 6, and 7) with publicly available expression data across multiple stages of development in maize (Wang et al., 2009b; Davidson et al., 2011), rice (Davidson et al., 2012), and Arabidopsis (Schmid et al., 2005) (Supplemental Table 2). We previously obtained 103 Robertson’s Mutator (Mu) insertions (Settles et al., 2007; McCarty et al., 2013) in 47 genes controlling auxin biosynthesis, transport, and signaling in maize, but none exhibited obvious morphological defects, illustrating the challenge of functional analysis in these highly redundant gene families with overlapping expression patterns. Construction of higher order mutants and the use of microRNA (miRNA) to target multiple genes have facilitated functional studies, and new gene-editing technologies will allow more effective targeting of multi-order loci, but knowledge of which genes are most closely related and expressed in which tissues is still essential. Therefore, the figures presented will aid selection of genes for future reverse genetic experiments in maize, rice, and Arabidopsis and move auxin research forward.

Auxin Biosynthesis Indole-3-acetic acid (IAA), the main form of natural auxin, is predominantly synthesized via a two-step, Trp-dependent TRYPTOPHAN AMINOTRANSFERASE of ARABIDOPSIS– YUCCA (TAA–YUC) pathway (Mashiguchi et al., 2011; Won et al., 2011). The first step of the pathway is the conversion of Trp to indole-3-pyruvate (IPA) by the TAA family of aminotransferases (Stepanova et al., 2008; Tao et al., 2008). The second and rate-limiting step is the conversion of IPA to IAA, which is catalyzed by the YUC family of flavin-containing monooxygenases (Stepanova et al., 2011; Dai et al., 2013). A number of Trp-independent (Wright et al., 1991; Normanly et al., 1993) and Trp-dependent (Zhao et al., 2001; Pollmann et al., 2003; Sugawara et al., 2015) pathways have been proposed, but the TAA–YUC pathway is currently the best understood auxin biosynthetic pathway in plants (Mashiguchi et al., 2011; Won et al., 2011). The TAA–YUC pathway is highly conserved across the plant kingdom (Gallavotti et al., 2008b; Phillips et al., 2011; Zhao, 2014) and traces its origin from charophyte algae (Romani,

Molecular Plant 2017). TAA and YUC enzymes are encoded by relatively small families of genes. In most plant genomes, the YUC gene family has more members than the TAA gene family (Poulet and Kriechbaumer, 2017). There are at least five TAA and 11 YUC genes in Arabidopsis (Chen et al., 2014), six TAAs and nine YUCs in maize (Gallavotti et al., 2008b; Chourey et al., 2010; Phillips et al., 2011), and four TAAs and 14 YUCs in rice (Zhang et al., 2018b). The TAA phylogenetic tree consists of two major clades (Figure 1A). One clade contains the Arabidopsis auxin biosynthetic genes, AtTAA1, AtTAA-RELATED1 (AtTAR1), and AtTAR2. These genes are joined by the well-characterized maize and rice auxin biosynthetic genes, VANISHING TASSEL2 (ZmVT2) (Phillips et al., 2011) and OsTAR2/OsFISH BONE (OsFIB) (Yoshikawa et al., 2014), respectively. The other clade includes alliinase-related genes, AtTAR3 and AtTAR4, along with at least two other maize and rice TAR genes with no confirmed enzymatic functions (Phillips et al., 2011; Kakei et al., 2017). The latter clade also includes a PpTAA gene, indicating an earlier specialization of alliinaserelated genes relative to auxin biosynthetic genes (Figure 1A). Consistent with previous phylogenetic analyses (Chourey et al., 2010; Phillips et al., 2011; Kakei et al., 2017), there is a clear divergence between auxin biosynthetic and alliinaserelated clades, as well as some degree of specialization among the gene members based on their expression patterns (Figure 1A). The YUC phylogenetic tree consists of four major clades (Figure 1B). The shoot-functional Arabidopsis YUC genes (Cheng et al., 2006) are found in two separate clades, with one clade containing AtYUC1 and AtYUC4 and the other containing AtYUC2 and AtYUC6. The maize YUC gene, SPARSE INFLORESCENCE1 (ZmSPI1) (Gallavotti et al., 2008b), which is mainly functional in inflorescence development, is in the same clade as AtYUC1 and AtYUC4. The root-functional AtYUC3, AtYUC5, AtYUC7, AtYUC8, and AtYUC9 (Chen et al., 2014) are found all together in a single clade. Interestingly, maize and rice YUC genes, which are highly expressed in the shoot, cluster together with these root-functional Arabidopsis genes, suggesting a potentially different function of grass YUC genes within this clade. It is also notable that there are maize and rice YUC genes that, unlike ZmSPI1, do not have clear co-orthologs in Arabidopsis. For example, the functionally characterized OsYUC8 (Woo et al., 2007; Fujino et al., 2008; Qin et al., 2017) clusters with ZmYUC7 in a monocot-specific subclade (Figure 1B) (Gallavotti et al., 2008b). The endosperm-specific ZmYUC1/ ZmDEFECTIVE ENDOSPERM18 (ZmDE18) (Bernardi et al., 2012) and OsYUC9 and OsYUC11 (Abu-Zaitoon et al., 2012) form a clade with AtYUC10 and AtYUC11, which have overlapping functions with AtYUC1 and AtYUC4 during embryo development (Cheng et al., 2007). The transmembrane domain structure and subcellular localization of YUC proteins have been proposed to correlate with specific tissue localization and function (Kriechbaumer et al., 2016; Poulet and Kriechbaumer, 2017). However, the existence of separate sets of shoot- and root-functional YUC genes have been sufficiently investigated only in Arabidopsis (Cheng et al., 2006, 2007; Chen et al., 2014), and functional evidence in monocot species remains scant. Molecular Plant 12, 298–320, March 2019 ª The Author 2019.

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Figure 1. Phylogenetic Trees and Transcript Expression across Tissues of TRYPTOPHAN AMINOTRANSFERASE (TAA) and YUCCA (YUC) Flavin-Containing Monooxygenase Enzyme Family Members. Approximately maximum-likelihood phylogenetic trees of (A) TAA and (B) YUC protein sequences from maize (green), rice (orange), and Arabidopsis (blue) with Physcomitrella (black) as an outgroup. The relative expression of each gene, mined from publicly available data, is depicted as a heatmap. To normalize for the different experiments, FPKM (maize and rice) and microarray data (Arabidopsis) values were converted to a percentage across tissues, so the heatmap indicates the highest (yellow) to lowest (blue) expression for each gene. To enable comparison of gene expression within a species, the average expression column was calculated for each gene by averaging the expression across all tissues, and then dividing by the average expression of all gene family members within a given species. Missing data or unrelated tissues across species are left blank. See Supplemental Table 2 and Supplemental Materials and Methods for detailed descriptions of tissue types and expression data (Schmid et al., 2005; Wang et al., 2009b; Davidson et al., 2011, 2012).

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Auxin EvoDevo Review In recent years, TAAs and YUCs have been implicated in the regulation of various developmental processes, including embryogenesis (Cheng et al., 2007; Stepanova et al., 2008), endosperm development (Abu-Zaitoon et al., 2012; Bernardi et al., 2012), root development (Stepanova et al., 2008; Pacheco-Villalobos et al., 2016; Zhang et al., 2018b), leaf expansion and vein formation (Cheng et al., 2007; Stepanova et al., 2008; Huang et al., 2017a; Kneuper et al., 2017), and inflorescence development (Cheng et al., 2006; Gallavotti et al., 2008b; Phillips et al., 2011). From what can be distilled from gene expression data (Figure 1A and 1B) and functional studies using knockout mutants, both TAAs and YUCs have specialized as well as overlapping biological functions within their respective families (Brumos et al., 2018). The severe pleiotropic phenotype in the Zmvt2 mutant in maize (Phillips et al., 2011) clearly demonstrates the developmental consequence of disrupting auxin biosynthesis. In maize, the male inflorescence, called the tassel, is found at the top of the plant and consists of a main spike with several lateral branches. One or several female inflorescences, termed ears, develop in the axils of leaves a few nodes below the tassel (McSteen, 2010). The Zmvt2 mutant has severely defective inflorescences with small and branchless tassels, while ears are reduced in size and number, and have fewer kernels (Phillips et al., 2011). These defects show that ZmVT2 functions in axillary meristem initiation and lateral organ formation during reproductive development in maize. In addition, Zmvt2 mutants also have fewer leaves (Phillips et al., 2011), defective vasculature (J. Robil and P. McSteen, unpublished data), reduced root branching (K. Phillips and P. McSteen, unpublished data), and longer primary roots (N. Best and P. McSteen, unpublished data), showing that ZmVT2 also has broad functions during vegetative development. Similarly, the loss of function of the OsTAR2/OsFIB gene in rice, a co-ortholog of ZmVT2 and ZmTAR2, results in a wide range of vegetative and reproductive defects (Yoshikawa et al., 2014). Osfib mutants show several root phenotypes that include longer seminal roots, fewer crown and lateral roots, and agravitropic responses (Yoshikawa et al., 2014). In addition, Ostar2/Osfib mutants exhibit an extremely dwarfed shoot with short, narrow, and adaxially rolled leaves (Yoshikawa et al., 2014). These phenotypes were recapitulated in CRISPR/Cas9 knockout lines providing further evidence that OsTAR2/OsFIB is the primary TAA gene for auxin biosynthesis in rice (Zhang et al., 2018b). Unlike maize, the male and female reproductive structures in rice are contained in bisexual spikelets along lateral branches of the terminal inflorescence (Gao et al., 2010). The Osfib mutant has significantly reduced inflorescence size and, in addition, has floral homeotic defects (Yoshikawa et al., 2014). These phenotypes are reminiscent of the rice tryptophan deficient dwarf1 (tdd1) mutant rescued by Trp supplementation (Sazuka et al., 2009). These observations indicate that vegetative and reproductive development in rice, like maize, relies mainly on IAA produced by Trp-dependent auxin biosynthesis. In Arabidopsis, various mutant screens have functionally characterized Attaa1 (Supplemental Table 1) in terms of shadeinduced responses and hormonal crosstalk (Stepanova et al., 2008; Tao et al., 2008; Chen et al., 2011; Zhou et al., 2011;

Molecular Plant Brumos et al., 2018). However, unlike Zmvt2 and Osfib, single mutants of Attaa1, Attar1, or Attar2 do not show developmental phenotypes under normal conditions (Stepanova et al., 2008). Higher order mutants, on the other hand, show dramatic developmental defects, whereby Attaa1 Attar2 double mutants have aberrant vasculature and floral structures, and Attaa1 Attar1 Attar2 triple mutants fail to develop a primary root, have reduced hypocotyl, and lack vasculature in cotyledons (Stepanova et al., 2008). Consistent with expression data (Figure 1A), this shows that TAA genes in Arabidopsis are broadly localized and are functionally redundant. Based on the expression patterns (Figure 1A), ZmVT2 and OsTAR2/ OsFIB may also have overlapping functions with their respective paralogs. However, this has not been validated in either maize or rice due to a lack of other taa-null mutants that show auxindeficient symptoms. Transposon insertion lines in ZmTAR1, ZmTAR2, and ZmTAR3 isolated from the maize Uniform-Mu population (Settles et al., 2007) exhibit no obvious defects (D. Coats, K. Marshall, and P. McSteen, unpublished data). Similarly, no null mutants have been generated for OsTAR1/OsFIB-LIKE (OsFBL), the only known paralog of OsTAR2/OsFIB in rice, although its aminotransferase activity has been confirmed (Kakei et al., 2017). Even though ZmVT2 shares a similar expression pattern with ZmTAR2 (Figure 1A), the severe vegetative and reproductive phenotypes of Zmvt2 mutants (Phillips et al., 2011) attest that it is the main TAA functional in auxin biosynthesis. ZmTAR1 and ZmTAR3, on the other hand, are highly expressed in endosperm development and, therefore, may not functionally overlap with ZmVT2 (Chourey et al., 2010) (Figure 1A). The Zmspi1 mutant is impaired in a single maize YUC gene, which is a co-ortholog of AtYUC1 and AtYUC4. Like Zmvt2, Zmspi1 has vegetative and reproductive phenotypes attributed to defects in axillary meristem and lateral organ initiation (Gallavotti et al., 2008b). While Zmspi1 mutants produce fewer leaves than normal plants, they have a more normal-looking stature than Zmvt2 mutants. This could indicate overlapping functions of ZmSPI1 with other ZmYUC genes during vegetative development (Gallavotti et al., 2008b) (Figure 1B). Reproductive defects in Zmspi1 mutants include tassels with fewer branches and spikelets and small ears with fewer kernels (Gallavotti et al., 2008b). The analysis of the Zmvt2 Zmspi1 double mutants in maize provided the first genetic validation for the TAA–YUC pathway in grasses (Phillips et al., 2011). The Zmvt2 Zmspi1 double mutants have only a slightly more severe phenotype and have the same free IAA levels as Zmvt2 single mutants, supporting that ZmVT2 and ZmSPI1 are in a linear auxin biosynthetic pathway (Phillips et al., 2011). Severe vegetative defects are associated with single loss-offunction yuc mutants in rice. Osyuc1 knockdown mutants display a severely dwarf phenotype (Yamamoto et al., 2007). A similar phenotype was observed in three mutant alleles of OsYUC8, which have been characterized for narrow, rolled leaf (Woo et al., 2007; Fujino et al., 2008) and reduced ethylene responses in roots (Qin et al., 2017). OsYUC1 and OsYUC8 likely resulted from a duplication event during the divergence of monocots and eudicots (Puhr, 2013). This may explain the resemblance of Osyuc1 and Osyuc8 mutant phenotypes and the similarity of their expression patterns (Figure 1B). Zhang et al. (2018b) Molecular Plant 12, 298–320, March 2019 ª The Author 2019.

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Molecular Plant generated overexpression lines of at least seven of the 14 YUC genes in rice. While the functions of individual YUC genes were not clearly delineated, it is noteworthy that overexpression of embryo- or seed-expressed YUC genes (OsYUC1, OsYUC3, OsYUC8, and OsYUC11; Figure 1B) leads to overproliferation of ectopic roots through activation of WUSCHEL-Related Homeobox 11, a regulator of cell fate transition during root organogenesis (Zhang et al., 2018b). Altogether, these genetic studies suggest overlapping functions of YUC genes in rice, though further investigations may uncover auxin biosynthesis modules for regulation of specific organ development. Unlike in maize and rice, loss-of-function mutations in single YUC genes in Arabidopsis do not show developmental defects. Severe defects are observed only in higher order YUC mutants (Cheng et al., 2006, 2007). For instance, dramatic progression of floral and leaf vascular defects is observed in Atyuc1 Atyuc4 double, Atyuc1 Atyuc2 Atyuc4 triple, and Atyuc1 Atyuc2 Atyuc4 Atyuc6 quadruple mutants (Cheng et al., 2006). The Atyuc1 Atyuc4 Atyuc10 Atyuc11 quadruple mutants fail to develop a hypocotyl and root meristem (Cheng et al., 2007). Analysis of different Atyuc mutant combinations reveals groups of YUC genes that are functional in either root or shoot development (Chen et al., 2014). However, it should be noted from gene expression data (Figure 1B) (Chen et al., 2014) that some exceptions might exist in these functional groupings. For example, AtYUC7, which is in the root-functional group, has a broad expression pattern, which is fairly high in shoot organs, while the shoot-functional AtYUC6 has strong expression in root tissues (Figure 1B) (Chen et al., 2014). The role of auxin in endosperm development may be very important in research aimed at improving yield in cereal crops. Previous studies have suggested that auxin biosynthesis directly affects endosperm development and grain filling in cereal grasses. The study of maize orange pericarp (orp) mutants, impaired in the Trp synthase b subunit, first suggested the possibility of a Trpindependent mechanism for IAA biosynthesis in maize kernels (Wright et al., 1991). Later, studies on endosperm-specific ZmTAR1 (Chourey et al., 2010) and ZmYUC1/ZmDE18 (Bernardi et al., 2012) provided evidence that both components of the Trp-dependent TAA–YUC pathway are essential for the high rate of auxin biosynthesis during maize endosperm development. Another example of modulation of seed growth by auxin biosynthesis is found in the maize miniature1 (mn1) mutant, where it was shown that the expression of ZmYUC1 is altered in response to sugar availability (LeClere et al., 2010). In rice, the expression of OsTAR1 and grain-specific OsYUC9 and OsYUC11 is found to be elevated during early grain development, coinciding with a significant increase in IAA and the start of the major starch deposition phase in grains (Abu-Zaitoon et al., 2012). Auxin biosynthesis is essential for correct endosperm initiation and development (Figueiredo et al., 2015, 2018). Thus, investigation of endosperm sub-functionalized TAAs and YUCs in cereal crops could potentially shed light on yield improvement.

Auxin Transport Auxin Transporters Auxin is transported from its sites of synthesis throughout the whole plant where it is required for a multitude of developmental processes. PAT has a strictly controlled directionality and occurs 302

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Auxin EvoDevo Review in a cell-to-cell fashion. Short-distance PAT in meristematic tissues causes the formation and maintenance of local auxin gradients required for organogenesis (Reinhardt et al., 2003). Long-distance PAT is the auxin flow through the whole plant body and controls apical dominance, among other responses. There are four known families of auxin transporters in plants: the PINFORMED (PIN) family, the PIN-LIKES (PILS) family, the ATP-binding cassette family B (ABCB)-P-glycoprotein (PGP) family, and the AUXIN1/LIKE-AUX (AUX/LAX) family (reviewed in Balzan et al., 2014; Grones and Friml, 2015). Members of these families are either polarly or non-polarly localized at the plasma membrane (PM) or in the endoplasmic reticulum (ER), and they are involved in auxin efflux, auxin influx, or both. Among those four families, the PIN family is the best characterized. In Arabidopsis, eight AtPIN family members (Supplemental Table 1) have been identified and functionally characterized €lweiler et al., 1998; Luschnig et al., 1998; (Chen et al., 1998; Ga Muller et al., 1998; Utsuno et al., 1998; Friml et al., 2002a, 2002b, 2003; Mravec et al., 2009; Simon et al., 2016). AtPINs encode integral membrane proteins with conserved hydrophobic membrane-spanning domains and a less conserved central hydrophilic loop of variable length (Krecek et al., 2009). Depending on the length of the hydrophilic loop, PINs are divided into the ‘‘long’’ AtPINs, which are usually involved in auxin efflux and localized at the PM, and the ‘‘short’’ AtPINs, which are typically localized at the ER and are thought to contribute to intracellular auxin homeostasis (Mravec et al., 2009; Cazzonelli et al., 2013). The PIN phylogenetic tree separates into two main clades; one contains AtPIN1 and the other harbors AtPIN5 and AtPIN8 (Figure 2). The AtPIN1 clade contains the long AtPINs, AtPIN2, AtPIN3, AtPIN4, and AtPIN7, while AtPIN5 and AtPIN8 have a shorter loop. In the PIN5–PIN8 clade, there is a one-to-one relation between maize and rice genes, while this is not consistently observed in the PIN1 clade (Figure 2). In addition, AtPIN6 splits off by itself before the branching of the two other clades (Figure 2). Recent research shows that AtPIN6 is ‘‘intermediate,’’ localizes to both the PM and the ER, and seems to have a dual role in both auxin transport and homeostasis (Simon et al., 2016). The Physcomitrella (Figure 2) and Selaginella (O’Connor et al., 2014) PINs form a sister group to angiosperm PINs, which indicates that before the split of monocots and eudicots, PIN family genes duplicated and were often retained. In both maize and rice, there are 12 PIN genes (Figure 2). In maize, three members cluster within the AtPIN1 subclade, namely ZmPIN1A, ZmPIN1B, and ZmPIN1C. In our tree, ZmPIN1D (also called ZmSisterofPIN1 [ZmSoPIN1]) is most closely related to AtPIN2 rather than AtPIN1 (Figure 2) (O’Connor et al., 2014). However, the Arabidopsis ortholog of ZmPIN1D was reported to have been lost (O’Connor et al., 2014). As ZmPIN1D/ ZmSoPIN1 appears to be a single-copy gene in maize, identifying and analyzing a Zmpin1d/Zmsopin1 mutant should be a focus of future research. There are three reported maize co-orthologs of AtPIN5 (ZmPIN5A, ZmPIN5B, ZmPIN5C), one ortholog of AtPIN8 (ZmPIN8), and three additional monocot-specific PINs (ZmPIN9, ZmPIN10A, ZmPIN10B) (Carraro et al., 2012; O’Connor et al., 2014; Yue et al., 2015). Similar observations were made for rice OsPINs (Wang et al., 2009a, 2018a). There are four PIN1 copies in rice. OsPIN1A and

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Figure 2. Phylogenetic Tree of PINFORMED (PIN) Auxin Exporter Family Members and Transcript Expression across Tissues. Approximately maximum-likelihood phylogenetic tree of PIN protein sequences from maize (green), rice (orange), and Arabidopsis (blue) with Physcomitrella (black) as an outgroup. The heatmap for gene expression comparison was generated as described in the legends of Figure 1.

OsPIN1B clustered with the AtPIN1 subclade, while OsPIN1C and OsPIN1D clustered with ZmPIN1D/ZmSoPIN1. There are three rice co-orthologs of AtPIN5 (OsPIN5A, OsPIN5B, OsPIN5C), one ortholog of AtPIN8 (OsPIN8), and three additional PINs (OsPIN9, OsPIN10A, OsPIN10B). Mining publicly available expression data and published literature indicates that members of the maize and rice PIN families show overlapping, as well as organ-specific, expression domains (Figure 2) (Carraro et al., 2006; Wang et al., 2009a; Forestan et al., 2010; Miyashita et al., 2010; Forestan and Varotto, 2012; Yue et al., 2015). When averaged across all tissues, the PIN1 clade members are expressed higher than the PIN5–PIN8 clade members (Figure 2). The PIN1 members are primarily expressed in shoots and inflorescences, with the exception of AtPIN2, which is highest expressed in the root. The PIN5–PIN8 clade is less uniform regarding expression domains, with different genes showing high expression in different tissues. For example, OsPIN5B is highly expressed in young seeds, while ZmPIN5B has its highest expression in stamens, which could suggest functional diversification (Figure 2). While AtPIN1 and ZmPIN1A are expressed in immature inflorescences, ZmPIN1B and ZmPIN1C show their

highest expression in pistils (Figure 2), suggesting subfunctionalization or functional diversification. In rice, OsPIN1A shows highest expression in shoots; OsPIN1B, OsPIN1C, and OsPIN8 in immature inflorescences; OsPIN1D in the embryo; OsPIN2 and OsPIN10A in pistils; OsPIN5A in the seedling; OsPIN5B, OsPIN5C, and OsPIN9 in young seeds; and OsPIN10B in mature inflorescences and stamens (Figure 2). Almost all (excluding OsPIN2 and OsPIN9) are induced by auxin treatments in roots (Wang et al., 2009a). While extensive functional studies of Atpin mutants and their phenotypes have been reported (Supplemental Table 1, reviewed in Balzan et al., 2014), this has not been the case for monocots. In maize, data on PIN family members comes from phylogenetic, expression, and protein localization studies (Carraro et al., 2006; Gallavotti et al., 2008a; Skirpan et al., 2009; Forestan et al., 2010, 2012; Yue et al., 2015). To date, functional characterization of Zmpin mutants is lacking due to the absence of mutations in all genes and the fact that single Zmpin mutants from the Uniform-Mu population (Settles et al., 2007) have so far not shown any obvious phenotypes (D. Coats and P. McSteen, unpublished data). The lack of phenotypes in Zmpin mutants is likely due to functional Molecular Plant 12, 298–320, March 2019 ª The Author 2019.

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Molecular Plant redundancy due to the duplication events highlighted above (Figure 2). However, confocal analysis of a ZmPIN1A:YFP fluorescent line and the rescue of the Atpin1 phenotype by ZmPIN1a suggest conservation of the PAT pathway between maize and Arabidopsis (Gallavotti et al., 2008a). Moreover, phosphorylation sites in ZmPIN1A are conserved in maize and Arabidopsis (Skirpan et al., 2009). Therefore, despite the lack of mutant data, ZmPIN1 function is likely conserved between maize and Arabidopsis. In rice, functional studies have been published for OsPIN1/ OsPIN1B/OsREH1 (a rice ETHYLENE INSENSITIVE ROOT1-like gene; Xu et al., 2005; Sun et al., 2018), OsPIN2/OsLARGE ROOT ANGLE1 (OsLRA1) (Wang et al., 2009a, 2018b; Miyashita et al., 2010; Chen et al., 2012; Wu et al., 2014; Inahashi et al., 2018), OsPIN10A/3a/3t (Zhang et al., 2012), and OsPIN5B (Lu et al., 2015) (Supplemental Table 1). RNAi knockdown and overexpression studies show that OsPIN1/OsPIN1B/ OsREH1 plays a role in adventitious root emergence and tillering (Xu et al., 2005). Recently characterized transfer DNA (T-DNA) insertion lines suggest an involvement of OsPIN1/ OsPIN1B/OsREH1 in the strigolactone and nitric oxidemediated elongation of seminal roots (Sun et al., 2018). Overexpression lines, as well as analysis of chemically induced mutations in OsPIN2/OsLRA1, indicate a role in tillering (Chen et al., 2012), mediation of root agravitropic responses (Wang et al., 2018b), and lateral root formation (Inahashi et al., 2018). The Ospin2/Oslra1 mutant also shows altered plant height under certain growing conditions (Wang et al., 2018b). Overexpression and knockdown experiments of OsPIN10A/3A/ 3t indicate a role in crown root development, tiller formation, and seed set (Zhang et al., 2012). OsPIN5B is the first rice PIN family member shown to localize to the ER (Lu et al., 2015) and to participate in both auxin transport and auxin homeostasis, thus indicating functional conservation between Arabidopsis and rice. Overexpression and knockdown experiments with OsPIN5B show its involvement in the control of plant height, leaf and tiller number, shoot and root biomass, seed setting rate, panicle length, and yield (Lu et al., 2015). These examples show how some functionalities are conserved between rice and Arabidopsis (e.g., both Atpin2 and Ospin2 mutants show developmental defects in roots). Although no obvious inflorescence phenotype has been reported in OsPIN1B lines, in contrast to Arabidopsis, where AtPIN1 is essential for flower development, it is likely that the four PIN1 copies in rice act redundantly in the inflorescence and that multi-order knockouts are needed. The AtABCB family comprises 22 family members in Arabidopsis (Balzan et al., 2014). ABCBs are a class of integral membrane proteins that actively transport various molecules across cellular membranes. Up to now, six members have been shown in Arabidopsis to be associated with auxin transport, namely AtABCB1, AtABCB4, AtABCB14, AtABCB15, AtABCB19, and AtABCB21 (Cho and Cho, 2013). AtABCB1 and AtABCB19 are involved in auxin efflux, while AtABCB4 and AtABCB21 are facultative auxin exporters/importers that control cellular auxin levels (Yang and Murphy, 2009; Kamimoto et al., 2012; Kubes et al., 2012). AtABCB14 is a malate transporter (Lee et al., 2008), but it was previously proposed that both AtABCB14 and AtABCB15 are also involved in auxin transport (Kaneda et al., 304

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Auxin EvoDevo Review 2011). Interestingly, the auxin-related ABCB transporters cluster into different phylogenetic clades (Cho and Cho, 2013) and show mainly non-polar PM localization, making them different from the AtPIN1 family of auxin exporters (Geisler et al., 2017). Many of the PpABCB genes group independently with Arabidopsis, maize, and rice rather than as an outgroup, indicating that multiple clades of ABCB were present in earlydiverging plants (Figure 3). The maize ZmABCB-PGP family is considerably larger than the AtABCB-PGP family, with 35 members (Yue et al., 2015). In rice, previous studies reported 22 or 24 putative OsABCB-PGP members (Garcia et al., 2004; Chai and Subudhi, 2016), comparable to the number in Arabidopsis. To visualize the relationship between these genes, we initially constructed an ABCB tree, which resulted in seven clades with distinct Physcomitrella genes that group separately into different subclades (data not shown). As three of these clades did not contain proteins shown to be involved in auxin transport, these clades were excluded from this analysis so that the ABCB tree depicted in Figure 3 consists of four major clades. Characterized auxin transporters do not group into one clade but are interspersed among these four major clades, as has been previously reported (Cho and Cho, 2013). These clades also contain uncharacterized ABCB transporters in Arabidopsis, maize, and rice. These uncharacterized ABCB genes should be a focus of future research to identify novel auxin transporters. Of the four clades, the AtABCB1 and AtABC19 subclade shows the highest average expression across tissues (Figure 3). While AtABCB1 and its co-orthologs in maize and rice show the highest expression in pistils, AtABCB19 has an additional expression domain in immature inflorescences (Figure 3). Co-orthologs of AtABCB19 show a high expression in immature inflorescences and some also in the embryo, indicating functional diversification. The three other clades depict a lower average expression and do not show an obvious trend toward specialized tissues. Functional characterization shows that single mutants in any of the AtABCB genes typically generate weaker phenotypes than mutants in AtPIN genes (Supplemental Table 1). The best characterized auxin-related AtABCBs are AtABCB1 and AtABCB19. AtABCB1 is involved in the regulation of plant height and hypocotyl development (Geisler et al., 2005; Ye et al., 2013) and also plays a role in anther development (Cecchetti et al., 2015). The Atabcb19 mutant shows dwarfism and altered cotyledon and root development, as well as altered tropic bending responses (Lin and Wang, 2005; Rojas-Pierce et al., 2007; Nagashima et al., 2008; Lewis et al., 2009; Christie et al., 2011). In addition, AtABCB19 acts synergistically with AtABCB1 during anther development (Cecchetti et al., 2015) and is involved in gravitropic responses of the inflorescence stem (Okamoto et al., 2016). In maize, functional studies have been reported for ZmABCB4, also known as ZmPGP1 and ZmBRACHYTIC2 (ZmBR2), which is an ortholog of AtABCB1. Zmbr2 mutants have a dwarf phenotype and bear the apical female ear at a lower node on the plant (Multani et al., 2003; Pilu et al., 2007; Knoller et al., 2010; Xing et al., 2015; Balzan et al., 2018). ZmAUX1 and ZmPIN9 have higher expression in Zmbr2 mutants, suggesting that different

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Figure 3. Phylogenetic Tree of Known Auxin Transporter ATP-BINDING CASSETTE-B (ABCB) and Related Proteins with Transcript Expression across Tissues. Approximately maximum-likelihood phylogenetic tree of selected ABCB protein sequences from maize (green), rice (orange), Arabidopsis (blue), and Physcomitrella (black). Due to high sequence diversity among the ABCBs, not all members of the family were included in the final tree (see Supplemental Materials and Methods). The heatmap for gene expression comparison was generated as described in the legends of Figure 1.

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Figure 4. Phylogenetic Tree of AUXIN1/LIKE-AUX (AUX/LAX) Auxin Importer Family Members and Transcript Expression across Tissues. Approximately maximum-likelihood phylogenetic tree of AUX/LAX protein sequences from maize (green), rice (orange), and Arabidopsis (blue) with Physcomitrella (black) as an outgroup. The relative expression of each gene, mined from publicly available data, is depicted as a heatmap. To normalize for the different experiments, FPKM (maize and rice) and microarray data (Arabidopsis) values were converted to a percentage across tissues, so the heatmap indicates the highest (yellow) to lowest (blue) expression for each gene. To enable comparison of gene expression within a species, the average expression column was calculated for each gene by averaging the expression across all tissues, and then dividing by the average expression of all gene family members within a given species. Missing data or unrelated tissues across species are left blank. See Supplemental Table 2 and Supplemental Materials and Methods for detailed descriptions of tissue types and expression data (Schmid et al., 2005; Wang et al., 2009b; Davidson et al., 2011, 2012).

auxin transporters compensate for the loss of ZmBR2 (Balzan et al., 2018). The plant height phenotype is observed in some Arabidopsis Atabcb1 alleles (Ye et al., 2013), showing conservation between ZmABCB4/ZmBR2 and AtABCB1. Phylogenetic analysis identified rice co-orthologs of AtABCB1 and AtABCB19 as OsABCB22 and OsABCB14, OsABCB16, respectively (Garcia et al., 2004; Knoller et al., 2010) (Figure 3). The Osabcb14 mutants are insensitive to 2,4dichlorophenoxyacetic acid (2,4-D) and IAA with respect to primary root length and shoot lengths (Xu et al., 2014), suggesting that OsABCB14 is required for auxin transport in both shoots and roots. Interestingly, the authors’ data showed an import or uptake function of OsABCB14 (Xu et al., 2014), which is surprising considering the close similarity to AtABCB1 and AtABCB19, suggesting functional diversification between rice and Arabidopsis. These differences in function also point to the possibility that ABCB members in maize and rice that cluster with non-auxin-related AtABCBs might have an auxin transport function and should be further investigated. A recent study identifying the malate transporter AtABCB14 as an auxin transporter further indicates this (Kaneda et al., 2011). While OsABCB14 and OsABCB16 show very similar expression patterns (Chai and Subudhi, 2016) (Figure 3), suggesting redundancy, other OsABCB family members were shown to exhibit complementary or even opposite expression patterns in the same tissue (Chai and Subudhi, 2016). The AtAUX1-LAX family members comprise a family of four highly conserved auxin import proteins, namely AtAUX1, AtLAX1, AtLAX2, and AtLAX3 (as reviewed in Swarup and Pe´ret, 2012), 306

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which show mainly non-polar localization at the PM (Cho and Cho, 2013). There are five AUX1-LAX genes in rice and in maize (Figure 4) and two gene duplications are thought to have occurred in the common ancestor of maize (ZmLAX1 and ZmLAX2; ZmLAX3 and ZmLAX5) and rice (OsLAX2 and OsLAX4; OsLAX1 and OsLAX3) (Figure 4) (Yue et al., 2015). The AUX1-LAX phylogenetic tree consists of two major clades (Figure 4) and the AtAUX1 and AtLAX1 clade shows the highest average expression across tissues. Across this clade, expression is highly diverse across tissues. ZmLAX3 and ZmLAX5 have their highest expression in young and developing seeds, while AtAUX1 has the highest expression in the roots, suggesting diversification of function within this clade (Figure 4). Members of the AtLAX2 and AtLAX3 clade have their highest expression primarily in inflorescences, with the exception of AtLAX3 (roots) and OsLAX2 (embryo). The AtAUX1-LAX gene family members have been shown to be involved in vascular transport, leaf positioning, and root stem cell patterning (Supplemental Table 1, reviewed in Swarup and Pe´ret, 2012). AtAUX1-LAX genes exhibit tissue-specific expression patterns and different functions. AtAUX1 is involved in the root gravitropic response and lateral root initiation (Marchant et al., 2002). AtLAX1, together with AtAUX1, regulates phyllotactic patterning and is involved in vascular development in cotyledons (Peret et al., 2012). AtLAX3 is necessary for proper lateral root development (Swarup et al., 2008). The functions of ZmAUX1-LAX family members have been inferred from expression (Hochholdinger et al., 2000) and transcriptome studies (Brooks et al., 2009). ZmAUX1 (ZmLAX2

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Auxin EvoDevo Review in Figure 4) is expressed in primary, lateral, seminal, and crown roots (Hochholdinger et al., 2000), but a mutant has not yet been identified. The first functional data for this family in maize come from a single Mu transposon insertion in ZmLAX3, which has agravitropic roots and mild defects in inflorescence branching (Huang et al., 2017b), thus indicating functions conserved with those of Arabidopsis. Notably, ZmLAX3 appears to have the highest expression within the gene family (Figure 4). Due to the lack of available mutants, the roles of other ZmAUX1-LAX family members remain elusive. Targeted gene editing approaches will help in future experiments as has been the case in rice (Wang et al., 2018c). OsAUX1-LAX genes show both ubiquitous and tissue-specific expression patterns (Chai and Subudhi, 2016) (Figure 4). OsLAX1/OsAUX1 controls many aspects of root development in rice (Yu et al., 2015; Zhao et al., 2015). Oslax1/Osaux1 knockout lines have an increase in primary root length and are insensitive to 2,4-D and IAA, while overexpression lines have shorter primary roots and are hypersensitive to 2,4-D and IAA (Yu et al., 2015). Recently an Oslax3/aux3 mutant was created using CRISPR/Cas9 technology, showing the involvement of OsLAX3 in the regulation of root development. Oslax3/aux3 mutants have shorter primary roots, decreased lateral root density, and longer root hairs and are insensitive to aluminum treatments (Wang et al., 2018c). It is interesting to note that, although OsLAX1/AUX1 and OsLAX3/AUX3 originated by duplication in grasses (Yue et al., 2015), their mutants show opposite phenotypes, suggesting functional diversification between these two genes. Interestingly, several OsLAX genes are expressed in the inflorescences of rice (Figure 4) but no flower phenotypes have been reported, whereas recently identified lax mutants in Setaria viridis and maize have reduced branching in the inflorescence (Huang et al., 2017b). However, the lack of Osaux1-lax mutants hinders a full understanding of the role of OsAUX1-LAX family members. Regulators of Auxin Transport Regulators of PAT in Arabidopsis have mainly been identified through identification of mutants, as well as from chemical studies using the chemical brefeldin A, which blocks endocytic recycling. Up to now, three regulatory systems for AtPINs have been described, namely control of polar localization, control of abundance at the PM, and control of biochemical activity. Detailed reviews about these regulators can be found elsewhere (Adamowski and Friml, 2015; Armengot et al., 2016). In maize, ZmBARREN INFLORESCENCE 2 (ZmBIF2) (McSteen et al., 2007) has been identified as the co-ortholog of AtPINOID, which was shown to control the localization of AtPINs by phosphorylation (Friml et al., 2004; Michniewicz et al., 2007) and the efflux activity of AtPINs (Zourelidou et al., 2014; Weller et al., 2017). ZmBIF2 phosphorylates ZmPIN1A (Skirpan et al., 2009), illustrating functional conservation between AtPID and ZmBIF2. However, ZmBIF2 also interacts with and phosphorylates ZmBARRENSTALK1 (ZmBA1) (Skirpan et al., 2008), indicating at least partial sub-functionalization, as AtPID has not been reported to interact with the Arabidopsis ortholog of ZmBA1, REGULATOR of AXILLARY MERISTEMS (ROX) (Yang et al., 2012).

In rice, one co-ortholog of AtPID, OsPID, and one OsPID-like gene have been identified (Morita and Kyozuka, 2007). OsPIDoverexpressing lines had no roots or thick roots, altered gravitropism response, altered floral development, and curled and stunted shoots. OsPID-like-overexpressing lines showed similar, but milder root phenotypes compared with OsPIDoverexpressing lines (Morita and Kyozuka, 2007), therefore showing at least partial redundancy between OsPID and OsPID-like. In contrast, AtPID-overexpressing lines show smaller and fewer rosette leaves and a thick vasculature system compared with their wild-type siblings (Saini et al., 2017). In addition, Christensen et al. (2000) show that AtPIDoverexpressing lines have either no or reduced lateral roots and a lack of gravitropic response, indicating some functional conservation between AtPID and OsPID.

Auxin Signal Transduction The known components of the canonical auxin signal transduction pathway include auxin co-receptors formed by TRANSPORT INHIBITOR RESPONSE1/AUXIN-RELATED F-BOX (TIR1/AFB) and Aux/IAA proteins, the transcriptional co-repressor TOPLESS (TPL), and the AUXIN RESPONSE FACTORs (ARFs) (Leyser, 2018). At low auxin levels, Aux/IAAs physically interact with ARFs and TPL, thereby preventing the expression of their target genes, likely due to a repressive chromatin status imposed by TPL-type co-repressors (Krogan et al., 2012). High intracellular auxin levels promote binding between Aux/IAAs and TIR1, which is part of an SCF E3-ubiquitin ligase complex, and trigger the degradation of Aux/IAAs, allowing ARFs, bound to specific DNA elements called auxin-responsive elements (AuxREs), to activate downstream target genes by first recruiting SWI/SNF chromatin remodeling factors (Wu et al., 2015; Weijers and Wagner, 2016). In this section, we discuss the functional analysis of the TIR1/AFB co-receptors, Aux/IAA repressors, and ARF transcription factors (Supplemental Table 1) but do not discuss other components of the signaling complex or direct targets due to space limitations. TIR/AFB Proteins The TIR1/AFB class of F-BOX proteins has been shown to bind auxin and facilitate degradation of the transcriptional repressor Aux/IAA proteins (Kepinski and Leyser, 2005). There are six members of the TIR1/AFB family in Arabidopsis, eight in maize, and five in rice (Figure 5). These family members arise from three subclades of TIR1/AFB genes, which pre-date the monocot/dicot divergence; however, gene copy number varies due to lineage-specific duplications in maize and Arabidopsis. For example, the ZmTIR1 and OsTIR1 genes are found as a single copy in maize and rice, respectively, while Arabidopsis has two copies (AtTIR1 and AtAFB1). In the AFB2/3 clade, there are two genes in Arabidopsis, two in rice, and three in maize, indicating duplications in all three lineages (Figure 5). The AFB4/5 clade, which has lower expression than the other clades and is proposed to bind picloram rather than IAA (Prigge et al., 2016), exhibits two additional maize duplications compared with rice, and all four maize genes have similar expressions, suggesting redundancy. Expression of TIR/AFB members appears to be widespread across species, with primarily high expression in inflorescences (Figure 5). However, maize genes in the AFB2/3 and AFB4/5 clades show higher Molecular Plant 12, 298–320, March 2019 ª The Author 2019.

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Figure 5. Phylogenetic Tree of TRANSPORT INHIBITOR RESPONSE1/AUXIN F-BOX (TIR1/AFB) Auxin Receptor Family Members and Transcript Expression across Tissues. Approximately maximum-likelihood phylogenetic tree of TIR1/AFB protein sequences from maize (green), rice (orange), and Arabidopsis (blue) with Physcomitrella (black) as an outgroup. The heatmap for gene expression comparison was generated as described in the legends of Figure 1.

relative expression in seeds compared with rice and Arabidopsis (Figure 5), which could suggest specialization of these genes in maize. The TIR/AFBs also contribute to the diversity of auxin responses by binding Aux/IAA with different affinities (Caldero´n-Villalobos et al., 2012; Pierre-Jerome et al., 2014). The Attir1 and Atafb mutants exhibit auxin-insensitive phenotypes that are much more evident in mutant combinations, especially Attir1 Atafb1 Atafb2 Atafb3 quadruple mutants (Parry et al., 2009), indicating redundancy in gene function (Supplemental Table 1). The TIR1/AFB auxin receptors have not been studied extensively in maize or rice. Mu insertions in the four maize genes most closely related to AtTIR1, AtAFB2, and AtAFB3 do not exhibit an obvious mutant phenotype (J. Struttmann and P. McSteen, unpublished data). In rice, overexpression of OsmiR393a and OsmiR393b results in down-regulation of OsTIR1, OsAFB2, and OsAFB2/3A (Xia et al., 2012), illustrating regulation conserved with that of Arabidopsis (Chen et al., 2011, 2015; Si-Ammour et al., 2011; Wang et al., 2018a). However, one miRNA is predominantly expressed in roots and the other in shoots, suggesting sub-functionalization (Bian et al., 2012). Plants overexpressing OsmiR393 exhibit auxindeficient phenotypes such as an increase in tiller production, hyposensitive responses to 1-naphthaleneacetic acid and 2,4-D in roots, and increased flag leaf inclination (Bian et al., 2012; Xia et al., 2012). OsTIR1 and OsAFB2 both physically interact with OsIAA1 and localize to the nucleus of onion epidermal cells (Bian et al., 2012) and OsTIR1 mediates auxin-induced degradation in yeast, illustrating functions conserved with those of Arabidopsis (Kanke et al., 2011; Pierre-Jerome et al., 2014). 308

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The TIR1/AFB proteins have been extensively investigated in Arabidopsis, showing that expression and function of AtTIR1 or AtAFB2 are necessary for auxin responses (Kepinski and Leyser, 2005; Parry et al., 2009; Wright et al., 2017) and that the SCFTIR1/AFB complex facilitates feedback regulation of auxin biosynthesis by regulating expression of the AtYUC genes (Takato et al., 2017). The Attir1-1, Atafb2-1, and Atafb3-1 mutants in Arabidopsis showed hyposensitivity to 2,4-D-induced root length inhibition and Attir1-1 had fewer adventitious roots (Dharmasiri et al., 2005), similar to what is observed in OsmiR393-overexpressing lines. Another similarity between rice and Arabidopsis in TIR1/AFB function is the effect on leaf morphology. The OsTIR1- and OsAFB2-RNAi lines exhibited altered leaf inclination (Bian et al., 2012), while Attir1-1 Atafb2-1 double mutants had an altered rosette leaf size (Dharmasiri et al., 2005). However, more studies are necessary to identify the conservation and/or diversification of TIR1/AFB function across plant evolution. AUXIN BINDING PROTEIN1 (ABP1) was originally shown to bind auxin and promote auxin-mediated cell expansion in maize and Arabidopsis (Lobler and Klambt, 1985; Palme et al., 1992; Steffens et al., 2001). However, it was recently revealed that newly developed mutants of AtABP1 do not affect auxin signaling nor development (Gao et al., 2015) and the originally identified Arabidopsis mutant phenotypes may be due to background mutations in PHYTOCHROME B (AtPHYB) and other genes (Dai et al., 2015; Enders et al., 2015). Auxindependent phenotypes in Atphyb mutants are not surprising, as both AtCRYPTOCHROME and AtPHYB have been recently

Auxin EvoDevo Review

Molecular Plant Figure 6. Phylogenetic Tree of AUXIN RESPONSE FACTOR (ARF) Family Members and Transcript Expression across Tissues. Approximately maximum-likelihood phylogenetic tree of ARF protein sequences from maize (green), rice (orange), and Arabidopsis (blue) with Physcomitrella (black) as an outgroup. Clade A (orange), clade B (blue), and clade C (gray) are color shaded and depicted on the left side of the phylogenetic tree. The heatmap for gene expression comparison was generated as described in the legends of Figure 1.

the phenotypes observed in maize Zmabp1 and Zmabp4 mutants, which were identified in highly Mu-active lines (Im et al., 2000; Borucka and Fellner, 2012; Jurisic-Knezev et al., 2012). Aux/IAAs and ARFs In higher plants, both ARF and Aux/IAA families have significantly expanded compared with earlier diverging plant lineages, and this may reflect the history of whole-genome duplications as well as the higher organismal complexity. For example, in rice there are 25 and 31 ARF and Aux/IAA genes, respectively (Jain et al., 2006; Wang et al., 2007), while the maize B73 genome contains 33 expressed ARF (Galli et al., 2018) and 34 Aux/IAA genes (Ludwig et al., 2013). In contrast, only one Aux/IAA and three ARF genes are present in Marchantia (Kato et al., 2015), and three Aux/IAA (Lavy et al., 2016) and 13 ARF genes are present in the Physcomitrella genome (Finet et al., 2013).

shown to bind AtAux/IAAs and inhibit their degradation and thus compete with AtTIR1/AFBs (Xu et al., 2018). The absence of a phenotype in Arabidopsis Atabp1 mutants brings into question

The ARF family invariably retains three evolutionarily conserved clades, A, B, and C (Finet et al., 2013; Flores-Sandoval et al., 2015; Galli et al., 2015, 2018) (Figure 6). While clade A ARFs fit well in the canonical auxin signaling pathway, less is understood about clade B and C ARFs. Clade B ARFs are generally considered repressors of transcription and contain a conserved repressor motif that drives interaction with TPL-type co-repressors (Causier et al., 2012). Recently, a functional study in Physcomitrella showed that competition of clade A and B ARF binding to their target genes may contribute to the fine-tuning of auxin signaling (Lavy et al., 2016), while it remains unclear if clade C ARFs function directly in the auxin signaling pathway (Flores-Sandoval et al., 2018). The ETTIN-like ARFs are a subclade of the B ARFs (Figure 6) and share a common repressor motif (Simonini et al., 2016). Moreover, some of the ETTIN-like ARFs have been proposed to act as non-orthodox auxin sensors (Simonini et al., 2016). The number of Arabidopsis genes in clade B is much higher compared with clades A and C (Figure 6), which could lead to functional redundancy and a greater degree of difficulty in characterization. Nevertheless, there appears to be tissuespecific expression of clade B genes, but the lack of functional Molecular Plant 12, 298–320, March 2019 ª The Author 2019.

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Molecular Plant data precludes other conclusions. No common trend regarding average expression between the clades was observed, except for the ETTIN-like subclade. In Arabidopsis, it has been shown that AtARF3/AtETTIN (AtETT) is involved in gynoecium development (Sessions and Zambryski, 1995); however, based upon expression of the maize and rice members, their function may be extended to embryo development in monocots (Figure 6). In recent years, several groundbreaking discoveries have greatly improved the understanding of the mechanisms by which auxin signal transduction components control transcription of target genes. Among these are the crystal structures of the ARF N-terminal domain bound to DNA (Boer et al., 2014), the Phox and Bem1 (PB1) C-terminal dimerization domain of ARFs (Korasick et al., 2014; Nanao et al., 2014), and the N-terminal domain of TPL-type co-repressors (Ke et al., 2015; Ma et al., 2017; Martin-Arevalillo et al., 2017). These crystal structures suggest that the formation of macromolecular complexes among ARFs, Aux/IAAs, and TPL co-repressor is highly likely and begin to address crucial questions on how the specificity of the auxin response is achieved during development. Crystal structures of two AtARF (AtARF1, clade B; AtARF5, clade A) DNA binding domains led to the caliper model in which the spacing of two adjacent AuxREs is a discriminant factor for DNA binding of different ARFs (Boer et al., 2014). Furthermore, in vivo evidence of ARF interactions with different types of transcription factors is starting to accumulate (Shin et al., 2007; Varaud et al., 2011; Oh et al., 2014; Jose Ripoll et al., 2015) and may contribute to cell and tissue type, as well as stage-specific responses, as originally suggested by bioinformatic analysis of AuxREs (Berendzen et al., 2012). Last, ARF interaction with SWI/SNF chromatin remodeling factors opens up the binding of additional transcription factors (Wu et al., 2015; Weijers and Wagner, 2016), which may also significantly contribute to the specificity of the auxin response. Functional analysis of ARFs has been particularly fruitful in Arabidopsis, whereby a series of clade A and B ARF functions has been revealed by loss-of-function mutations in single or double mutant combinations (Supplemental Table 1). For example, recent studies have revealed clade A AtARF6 and AtARF8 function in fruit valve growth by regulation of AtAPETALA2 (AtAP2) in conjunction with the MADS-box protein AtFRUITFULL (AtFUL) (Jose Ripoll et al., 2015); clade A AtARF5/AtMONOPTEROS (AtMP) regulates the expression of three paralogous transcription factors required for the initiation of the root meristem during embryogenesis (Crawford et al., 2015); and AtARF3/AtETT, a non-canonical ARF missing the PB1 dimerization domain, regulates floral meristem determinacy (Zhang et al., 2018a). Furthermore, another study on AtARF3/AtETT regulation of fruit development led to the discovery of an alternative auxin signaling pathway involving auxin-dependent disruption of AtARF3/AtETT interaction with different transcriptional regulators (Simonini et al., 2016). Whether this pathway is conserved in other species is unknown. Recently, genome-wide analysis of maize clade A and B ZmARF DNA binding behavior revealed several differences in binding properties between the phylogenetically distinct clades for motif recognition, binding site location, and genomic distribution, and suggested that clade B ZmARFs may contribute to auxin 310

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Auxin EvoDevo Review signaling in both a competitive and a cooperative fashion (Galli et al., 2018). While these results stemmed exclusively from DNA affinity purification sequencing, an in vitro approach (O’Malley et al., 2016), and did not take into account possible heterodimer formation, this nonetheless suggests that ARFs belonging to the same clade have very similar DNA binding properties and that the specificity of the auxin response derives from factors other than ARF binding alone (Galli et al., 2018). So far, only scant functional evidence is available for both rice and maize ARFs. Among these, an miRNA-resistant version of clade C OsARF18 showed pleiotropic defects affecting rice stature, leaf, and seed development (Huang et al., 2016). Similarly, miRNA regulation of the Arabidopsis co-ortholog AtARF10 has been implicated in seed dormancy, leaf, and fruit development (Liu et al., 2007). In another instance of partial functional conservation between rice and Arabidopsis, overexpression of clade A OsARF19 produced rice plants with a dramatically changed leaf angle, due to increased adaxial cell division in the lamina (Zhang et al., 2015). The phylogenetically related AtARF19 in Arabidopsis (Figure 6) regulated root hair elongation in response to low phosphate (Bhosale et al., 2018), and in combination with its paralog AtARF7/AtNPH4 controlled lateral root formation and leaf expansion (Wilmoth et al., 2005). In maize, clade A ZmARFs have largely overlapping expression patterns and, due to a higher number of genes, functional redundancy appears to be more extensive than in Arabidopsis and rice (Galli et al., 2015). In our experience, a collection of transposon insertions (Settles et al., 2007) in 12 of 13 maize clade A ZmARF genes expressed in inflorescences failed to reveal any obvious phenotype (Q. Liu and A. Gallavotti, unpublished data). Since this clade contains several closely duplicated genes (Figure 6), the availability of new gene-editing tools for maize should also help to generate higher order mutants and overcome redundancy. Aux/IAAs are short proteins with variable sequences but welldefined and conserved domains (Weijers and Wagner, 2016). The Aux/IAA phylogenetic tree has nine clades (I–IX; indicated for ease of description in this review) with two monocotspecific clades (clade I and V) and one Arabidopsis-specific clade (clade IX; Figure 7). Clade VI and clade VIII showed the highest average expression across tissues, while clade III showed the lowest expression. Clade VI contains AtIAA14/ AtSOLITARY ROOT (AtSLR), AtIAA7/AtAUXIN RESISTANT2 (AtAXR2), and AtIAA17/AtAXR3. Arabidopsis members of this clade are highly expressed in the root; however, this does not hold true for members from maize. Genes in clade VI are also highly expressed in the pistils, except for AtAXR3. Clade VIII contains AtPAP2, and Arabidopsis members of this clade are highly expressed in developing seeds, while monocot members of this clade are not (Figure 7). Characterized maize members with similar phenotypes fall into separate clades (e.g., ZmIAA27/ZmBIF1 and ZmIAA20/ZmBIF4), which implies that relying solely on phylogenetic analyses to decide which genes to study using reverse genetic approaches to overcome redundancy is not sufficient. Knowledge of expression across tissues is also needed before creating multi-order knockout mutants.

Auxin EvoDevo Review

Molecular Plant Figure 7. Phylogenetic Tree of AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) Transcription Repression Factor Family Members and Transcript Expression across Tissues. Approximately maximum-likelihood phylogenetic tree of Aux/ IAA protein sequences from maize (green), rice (orange), and Arabidopsis (blue) with Physcomitrella (black) as an outgroup. Respective clades are named and color shaded on the left side of the phylogenetic tree to facilitate description for this article. Clade I (shaded in blue), clade II (dark orange), clade III (green), clade IV (red), clade V (gray), clade VI (light orange), clade VII (purple), clade VIII (dark blue), and clade IX (yellow) are shown. The heatmap for gene expression comparison was generated as described in the legends of Figure 1.

meristem1 (ZmRum1), ZmBif1, and ZmBif4 (von Behrens et al., 2011; Galli et al., 2015). While ZmRum1 mutants show reduced lateral root development and defects in vasculature organization (Zhang et al., 2014), ZmBif1 and ZmBif4 specifically affect organogenesis, resulting in inflorescences lacking branches and spikelets due to failure to initiate bract primordia and subtending axillary meristems. Confocal imaging of a ZmPIN1A:YFP reporter in ZmBif1 ZmBif4 double mutant tassels shows that PAT-driven patterning is completely disrupted in these plants (Galli et al., 2015). Based on phylogenetic relationships, ZmIAA27/ZmBIF1 and ZmIAA20/ZmBIF4 are co-orthologous to AtIAA15 and AtIAA28, respectively, while the ZmIAA10/ZmRUM1 phylogenetic position is less obvious from our tree (Figure 7). Based on previous analysis, ZmIAA10/ZmRUM1 may be closely related to three Arabidopsis Aux/IAA genes, AtIAA8, AtIAA9, and AtIAA27 (Galli et al., 2015). Overexpression of AtIAA15 in Arabidopsis shows a range of pleiotropic phenotypes, such as shorter inflorescences, small curled leaves, and defective root gravitropic response, while miRNA-guided knockdown lines show no differences compared with wild-type plants (Yan et al., 2013). In contrast to ZmIAA20/ZmBIF4, AtIAA28 is not auxin inducible and a gain-of-function mutation specifically affects lateral root formation and plant stature (Rogg et al., 2001). In addition, it was recently shown that AtIAA28 mRNA is under miR847 regulation and its cleavage promotes auxin-mediated lateral organ development (Wang and Guo, 2015). These examples highlight several functional differences between putative orthologous genes in maize and Arabidopsis for ZmIAA27/ZmBIF1 and ZmIAA20/ ZmBIF4, while the ZmIAA10/ZmRUM1 function appears to be conserved, since AtIAA8 is reported to be involved in lateral root formation (Arase et al., 2012).

Functional data on the role of auxin signaling in maize root and inflorescence development come from the analysis of semidominant Zmaux/iaa mutants, such as Rootless with undetectable

In rice, the majority of reported phenotypes in Aux/IAA genes are due either to stabilizing mutations in the well-conserved degron domain, responsible for auxininduced degradation, or to overexpression studies. Commonly observed phenotypes include defects in root and tiller development. For example, overexpression of OsIAA4 causes increased tiller angle and reduced plant height and perturbs the response of roots to treatments with 2,4-D (Song and Xu, 2013). Overexpression of the rice OsIAA6 gene improves drought tolerance, while a knockdown mutant Molecular Plant 12, 298–320, March 2019 ª The Author 2019.

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Molecular Plant caused by a T-DNA insertion increases tiller number by derepression of axillary bud outgrowth along the main stem. Homozygous mutants for the insertion could never be obtained due to seed abortion (Jung et al., 2015). This represents a rare case of a loss-of-function mutation in an Aux/IAA gene that is reported to produce a visible phenotype, although it is unclear if additional insertions were present in this line. OsIAA9 regulates root gravitropism when overexpressed in Arabidopsis seedlings (Luo et al., 2015), while stabilized OsIAA13 causes a reduction in lateral root formation and defective gravitropic responses (Kitomi et al., 2012). Interestingly, the cis/trans isomerization of a closely related Aux/IAA protein, OsIAA11, was also shown to affect its stability and perturb lateral root formation in rice seedlings (Zhu et al., 2012; Jing et al., 2015). OsIAA11 and OsIAA13 are closely related to a group of Arabidopsis Aux/IAA genes including AtIAA14/AtSLR (Figure 7), whose stabilized protein also blocks lateral root formation in Arabidopsis (Fukaki et al., 2005). Semi-dominant stabilizing mutations in OsIAA23 affect root development, due to failure to maintain the quiescent center, and shoot development (Jun et al., 2011). These mutations were used for a genetic screen for revertants that led to the identification of a series of critical amino acids in the PB1 domain that when mutated abolish interaction with OsARFs (Ni et al., 2014). Crucially, when the same conserved residue was mutated in several OsARF proteins, the Osiaa23 phenotype could be rescued to some degree (Ni et al., 2014), suggesting that several OsARFs, perhaps not surprisingly, function redundantly in root and shoot development.

CONCLUSIONS AND FUTURE PERSPECTIVES Mining publicly available expression data and reviewing recent functional studies showed cases of both conservation and diversification between and within species in all components of the auxin cascade. Functional conservation and redundancy have created significant challenges in studying gene function utilizing classical genetic techniques. Specifically, subtle phenotypes and variable phenotypic penetrance make these experiments difficult. Therefore, multi-order mutants are needed in both maize and rice, as has been done in Arabidopsis, to overcome these limitations and obtain a better understanding of the functional roles of auxin gene family members. In the past, reverse genetic research in maize primarily involved using transposon mutagenesis systems (McCarty and Meeley, 2009). Applying a Mu approach to gene family members controlling auxin biosynthesis, transport, and signaling was not successful (D. Coats, P. McSteen, and A. Gallavotti, unpublished data).There are several possible reasons for this: Mu elements primarily target 50 untranslated regions and do not necessarily knock out gene function (Dietrich et al., 2002), Mu alleles are sometimes dependent on Mu activity for expression (Lisch, 2013, 2015), and there is extensive overlapping expression of related gene family members, as is evident from mining publicly available expression data (Figures 1, 2, 3, 4, 5, 6, and 7). We envision that the ability to perform CRISPR/Cas9 knockout of multiple related gene family members (Xing et al., 2014; Svitashev et al., 2015) together with the advancement of high-throughput 312

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Auxin EvoDevo Review phenotyping methods in crop species (as reviewed in Rebetzke et al., 2016) will dramatically advance functional research on these highly redundant gene family members in maize. Recent developments in maize transformation technologies, and in particular the ability to directly transform the maize inbred line B73, would significantly speed up this approach if the technology became widely available (Lowe et al., 2016; Mookkan et al., 2017). Generating knockout lines and higher order mutants using CRISPR/Cas9 has already been optimized in rice (Zhang et al., 2018b; Li et al., 2018) and will advance auxin research by providing more accurate functional information than the more widely used overexpression and RNAi studies. Recent developments in fluorescent marker design in both maize (Wu et al., 2013; Krishnakumar et al., 2015) and rice (Yang et al., 2017), specifically the development of fluorescent auxin biosensors (Mir et al., 2017; Yang et al., 2017), have greatly improved molecular and functional characterization approaches of auxin genes in monocots. Functional studies will further profit from newly developed biochemical inhibitors that, in addition to the currently available auxin transport inhibitors, now enable various aspects of auxin biosynthesis and signaling to be inhibited (Hasegawa et al., 2018; Ma et al., 2018). In addition, recent developments of the orthogonal convex– concave auxin–TIR1 pair (Torii et al., 2018) and synthetic auxin yeast systems (Havens et al., 2012; Pierre-Jerome et al., 2013, 2014, 2016) will allow for further investigation of conservation and diversification of auxin signaling, bypassing issues of redundancy. Altogether, these biotechnological advances should greatly facilitate future auxin research in maize, rice, and other crop species.

SUPPLEMENTAL INFORMATION Supplemental Information is available at Molecular Plant Online.

FUNDING This research was supported by the National Science Foundation, Plant Genome Research Program IOS-1114484/0820729 to P.M., S.M., and A.G. and IOS-1546873 to P.M. and A.G.

AUTHOR CONTRIBUTIONS M.S.M. and N.B.B. extracted and compiled expression data. S.M. constructed initial phylogenetic trees and N.B.B. constructed the trees presented in the figures. M.S.M., N.B.B., J.M.R., A.G., and P.M. wrote the manuscript. All authors approved the final version of the manuscript.

ACKNOWLEDGMENTS We would like to apologize to colleagues whose work could not be cited due to space constraints. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. The authors do not have any financial conflicts of interest. Received: September 4, 2018 Revised: December 2, 2018 Accepted: December 16, 2018 Published: December 24, 2018

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