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First published online July 14, 2006; 10.1104/pp.106.080119 Plant Physiology 142:254-264 (2006) © 2006 American Society of Plant Biologists ZmPIN1a and ZmPIN1b Encode Two Novel Putative Candidates for Polar Auxin Transport and Plant Architecture Determination of Maize1,[W]Dipartimento di Agronomia Ambientale e Produzioni Vegetali, Università degli Studi di Padova Agripolis–Viale dell'Università 16, 35020 Legnaro (PD), Italy (N.C., C.F., S.C., S.V.); and Laboratoire de Reproduction et Développement des Plantes, École Normale Supérieure-Lyon, 69364 Lyon, France (J.T.)
Shoot apical meristems produce organs in a highly stereotypic pattern that involves auxin. Auxin is supposed to be actively transported from cell to cell by influx (AUXIN/LIKE AUXIN proteins) and efflux (PIN-FORMED proteins) membrane carriers. Current hypotheses propose that, at the meristem surface, PIN proteins create patterns of auxin gradients that, in turn, create patterns of gene expression and morphogenesis. These hypotheses are entirely based on work in Arabidopsis (Arabidopsis thaliana). To verify whether these models also apply to other species, we studied the behavior of PIN proteins during maize (Zea mays) development. We identified two novel putative orthologs of AtPIN1 in maize and analyzed their expression pattern during development. The expression studies were complemented by immunolocalization studies using an anti-AtPIN1 antibody. Interestingly, the maize proteins visualized by this antibody are almost exclusively localized in subepidermal meristematic layers. Both tassel and ear were characterized by a compact group of cells, just below the surface, carrying PIN. In contrast to or to complement what was shown in Arabidopsis, these results point to the importance of internally localized cells in the patterning process. We chose the barren inflorescence2 (bif2) maize mutant to study the role of auxin polar fluxes in inflorescence development. In severe alleles of bif2, the tassel and the ear present altered ZmPIN1a and ZmPIN1b protein expression and localization patterns. In particular, the compact groups of cells in the tassel and ear of the mutant were missing. We conclude that BIF2 is important for PIN organization and could play a role in the establishment of polar auxin fluxes in maize inflorescence, indirectly modulating the process of axillary meristem formation and development.
Plant architecture is defined by the combination of external and internal cues, which determine the expression pattern of developmental genes. The shoot apical meristem (SAM) generates the aerial part of the plant. It carries a group of totipotent stem cells, which are capable of self perpetuation and, at the same time, can differentiate as daughter cells and participate in the formation of the primordia. The SAM is formed during embryogenesis and produces modular units, called phytomers. The spatial and temporal arrangement of lateral organs around the main axis is defined as phyllotaxis. This process is highly repetitive and depends on the species and developmental stage (Traas and Vernoux, 2002  ; Traas and Bohn-Courseau, 2005; Carraro et al., 2006).
During vegetative growth, maize (Zea mays) produces several axillary meristems (AMs) along its stem. After the switch to the reproductive phase, plants carry a male inflorescence, called the tassel, at the tip of the main axis, and a female inflorescence, called the ear, at the axil of a leaf between the fourth and the seventh node. The tassel is highly branched with longer lateral branches at the base, produced by branch meristems (BMs), and it bears unisexuate male flowers (Irish, 1997
It has recently been demonstrated that auxin plays a major role in meristem function. In particular, polar auxin transport (PAT) is implicated in lateral organ initiation at the SAM in Arabidopsis (Arabidopsis thaliana), where it determines the position of flowers and leaves around the inflorescence stem (Reinhardt et al., 2000 In this study, we analyze the expression pattern of two putative AtPIN1 orthologs, ZmPIN1a and ZmPIN1b, in the SAM, tassel, and ear of maize. We also investigate the possible role of PAT in the initiation and differentiation of maize inflorescences through localization of putative auxin efflux transporters in wild-type plants and in the barren inflorescence2 (bif2) mutant. Taken together, our results suggest that ZmPIN1a and ZmPIN1b play a fundamental role in meristem function and point to a role for the internal tissues in organ positioning. In addition, they suggest a role for internal meristematic tissues in the patterning process, in contrast to what was proposed for Arabidopsis.
ZmPIN1a and ZmPIN1b: Two PIN1-Like Genes from Maize To identify maize PIN1-like genes belonging to the PIN family of putative auxin efflux carriers, we screened the National Center for Biotechnology Information (NCBI), The Institute for Genomic Research (TIGR), and Maize Genetics and Genomics Database (MaizeGDB) using the AtPIN1 (AT1G73590 for genomic DNA and AF089084 for cDNA) sequences as a query. Thirty maize tentative unique contig sequences were collected. Primers designed using the retrieved sequences were employed in PCR and reverse transcription (RT)-PCR assays to obtain maize PIN1-like (ZmPIN1) genes and cDNAs. Two full-length genomic sequences of 2,649 and 2,521 bp were identified and named ZmPIN1a and ZmPIN1b, respectively. The ZmPIN1a (accession no. DQ836239) corresponding cDNA is 1,806 bp long and encodes a putative protein of 601 amino acids (65.2 kD). The ZmPIN1b (accession no. DQ836240) corresponding cDNA is 1,788 bp in length and its open reading frame (ORF) encodes a putative protein of 595 amino acids (64.5 kD; Fig. 1A ). The amino acid identity between the putative maize proteins is 86.7%. The main difference in both the genomic and putative protein sequences between the two maize members is due to a 44-bp insertion at the end of the first exon in ZmPIN1b corresponding to the hydrophilic domain in the putative protein (Fig. 1C). The two maize genes showed an intron-exon structure comparable to that of AtPIN1 (Fig. 1A). The AtPIN1 protein exhibits an amino acid identity of 70.4% and 70.9% with ZmPIN1a and ZmPIN1b, respectively (Fig. 1C).
The two maize PIN1-like proteins and AtPIN1 showed a similar hydropathy profile, with two putative lipophilic domains at the N and C ends and one central hydrophilic loop (Fig. 1B). To determine the similarity of our two putative PIN sequences in relation to the PINs of Arabidopsis and other plant species, we constructed a neighbor-joining phylogenetic tree with 100 bootstrap using Phylip, including PIN-like amino acid sequences from wheat (Triticum aestivum), rice, and Arabidopsis. The resulting schematic representation was drawn using Tree-View 1.6.6 (for details, see "Materials and Methods"). ZmPIN1a and ZmPIN1b fall in the same cluster as the putative PIN1 of Arabidopsis, rice, and wheat (Fig. 2 ).
Expression Patterns To analyze the expression of ZmPIN1a and ZmPIN1b, we performed semiquantitative RT-PCR using RNA extracted from different tissues: roots, seedlings, leaves, tassels, and ears of B73. Specific combinations of primers were used to selectively amplify ZmPIN1a or ZmPIN1b and ubiquitin as controls of the expression levels. ZmPIN1a and ZmPIN1b showed differential expression, according to the tissues and developmental stage considered. No significant differences could be observed between ZmPIN1a and ZmPIN1b expression in roots, seedlings, leaves, and tassels of B73. ZmPIN1a was not present in young ears, whereas the transcripts could be detected at a later stage of development. ZmPIN1b was also expressed in young ears and later its expression increased during development of the female inflorescence (Fig. 3 ).
Expression and Localization of ZmPIN1a and ZmPIN1b in Vegetative and Reproductive Tissues In situ hybridization with a ZmPIN1 antisense probe was employed to assess the localization of ZmPIN1 mRNA in different maize tissues. The probe was supposed to hybridize to both ZmPIN1a and ZmPIN1b mRNAs. In the mature embryo, ZmPIN1 RNA was present in a few cells positioned in the central region of the apical-basal axis. The signal was also present in the cells forming the border between the two lateral primordia of the seminal roots and the main axis of the embryo. No signal was visible in the embryonic SAM and in the embryonic leaves or cotyledon (scutellum; data not shown). In the root, the hybridization signal was mainly detected in the central cylinder and a weaker signal was detected in the cortex (data not shown). In seedlings and young maize plants, ZmPIN1 transcripts were present in inner cells of the SAM itself, in the lateral outgrowing primordia, and in the tips of young leaves (Fig. 4A ). It was also strongly expressed in the vascular bundles of the apex and leaves.
In maize, after the transition to flowering takes place, the SAM differentiates into a tassel (Fig. 4). At the beginning of tassel differentiation, the ZmPIN1 mRNAs localized at the top of the tassel in the vascular bundles of the inflorescence axis and at the place of BM initiation (Fig. 4, B and C). When the AMs differentiated into SMs, the localization of the transcripts became restricted to the apical cells of the elongating SMs, supposedly along the differentiating provascular strands (Fig. 4, D–F). The same expression pattern was repeated in the lateral branches of the tassel, where the transcript was first detected at the top of the BM and then in the vascular bundle of the branch axis and in the main axis of the elongating SM (Fig. 4, G and H). In developing ears, the expression was detected in lateral bracts, at the tip of bract primordia, in the vasculature and central cells of the inflorescence meristem, but not in the cells forming the outermost layer of the meristematic dome (Fig. 5 , A and B). At later stages of development, the signal appeared to spread over the whole top of the upper part of the ear (the same as in the tassel) and was again localized in the AMs (Fig. 5C). Later on, the ZmPIN1 mRNA was detected in the spikelet glumes and axis of the two forming florets (Fig. 5, D and E).
ZmPIN1 Protein Localization
To determine the localization of ZmPIN1 proteins, we performed immunostaining experiments using an anti-AtPIN1 antibody on tissues from the B73 inbred line. This antibody has been characterized (Boutté et al., 2006
ZmPIN1 proteins were also localized in the SAM dome. Here, polar localization of the proteins appeared at the basal end of the central cells, whereas no labeling was observed in the L1 and outer layers. Furthermore, polarization was evident in the vasculature of the leaves and, most of all, at the position of young forming lateral primordia (Fig. 7 , A and B). When the SAM switched from the vegetative to the reproductive phase, ZmPIN1 proteins localized in the apical region of the developing tassel, just below the surface (Fig. 7, C–F; Supplemental Fig. 2). In some of these subapical cells, the PIN orientation was not strictly basal, but other orientations were observed as well. Along the tassel axis, PIN labeling was observed in two parallel cell files. Here, the polarization pattern suggested an auxin flux directed downward toward the base of the stem (Fig. 7D; Supplemental Fig. 2). The stained cells corresponded to the provasculature. Later on, the tassel vasculature clearly differentiated and staining was present in all the vascular bundles of the tassel central axis. Cross sections (data not shown) and longitudinal sections of the young tassel indicated that the signal remained confined to the inner cells and never interested the outer layers (Fig. 7, C, E, and F). Finally, when the tassel produced SMs, the pattern appeared more complex and we detected several relocalizations of the putative ZmPIN1 (Fig. 7, G and H). The signal was evident during spikelet differentiation, first along the cells that will form the central axis of the spikelet. Successively, the two florets are produced by the FMs and ZmPIN1 proteins are visible within their central cells. At a later stage of development, ZmPIN1 proteins localized at the site of the lower spikelet glumes, pointing toward the tassel central axis (data not shown). In the young female inflorescence, the expression pattern of ZmPIN1 appeared very similar to that of the young tassel (Fig. 7I; Supplemental Fig. 3). The signal was clearly visible in the vasculature and at the place of primordia bulging from the SMs. When the SMs produced spikelets, the proteins could be detected again in the lower glumes, in the vasculature, and also in the developing florets (Fig. 7, J and K). For the negative controls of immunostaining experiments, see Supplemental Figure 1.
ZmPIN1 Expression in bif2
Localization of ZmPIN1 transcripts and proteins were determined in the bif2 mutant. The most severe alleles of this mutant present extremely reduced branching, both in male and female inflorescences, although plant bodies are normally developed (McSteen and Hake, 2001 RT-PCR experiments conducted on RNA from bif2 tissues demonstrated that the levels of expression of ZmPIN1a and ZmPIN1b are similar to those of wild-type maize in roots and seedlings, whereas ZmPIN1a is more expressed in mutant tassels (Fig. 3). In situ hybridization experiments on bif2 vegetative apexes showed that transcript localization in the SAM resembles that of the wild-type B73 inbred line (data not shown). Moreover, immunolocalizations showed that the ZmPIN1 proteins in the mutant vegetative SAM followed a regular pattern (Fig. 8A ). The anatomy of the mutant male inflorescence was analyzed in detail and the most severely affected tassels presented a highly irregular vasculature and an epidermis-like tissue forming the outermost layer. On this outer layer we found the presence of structures typical of a leaf epidermis, such as stomata and hairs (Fig. 8, C and D). Immunolocalization experiments indicated that there was no ZmPIN1 protein detection at all in the tassel of severe mutants, neither at the tip nor in the central vascular tissues (Fig. 8B). At the same time, polarization of ZmPIN1 proteins in the leaf vasculature of the same plants was evident (data not shown). Similar results were observed in the ears, with the disruption of the vasculature pattern in the central axis, but not in the leaves (Fig. 8E). Here, a few lower spikelets were formed and they presented abnormal/normal ZmPIN1 expression. Most of the ear surface did not differentiate SMs and, at the place where we expected to find these structures, an important difference was that ZmPIN1 did not appear in the central part of the SM, as observed in the wild type. A large domain, including the whole tip of the ear, presented polarized labeling, with the ZmPIN1 protein basally inserted into the plasma membrane of all cells, even in the surface layer.
ZmPIN1a and ZmPIN1b Are Homologs of AtPIN1
The ORF of ZmPIN1a and ZmPIN1b encodes putative polypeptides with 71.3% and 70.9% identity to AtPIN1, respectively. Phylogenetic analysis shows that ZmPIN1a and ZmPIN1b fall into the same cluster together with the orthologous PIN1 proteins of rice, Arabidopsis, and wheat. Hydropathy profiles revealed that the PIN1 proteins contain two blocks of transmembrane segments connected by a hydrophilic region (Galweiler et al., 1998 Although semiquantitative RT-PCR reveals that the two genes show similar expression levels in roots, seedlings, leaves, and tassels of B73 plants, differences are observed as well. ZmPIN1a, for example, is not expressed in young ears, where only ZmPIN1b is present. This demonstrates diversification of the domains of expression, with ZmPIN1a more expressed in tissues carrying several vascular bundles as leaves and differentiated ears. At the same time, ZmPIN1b appears to be more specific for young ears and tassels.
In the male and female inflorescences, ZmPIN1 expression patterns are strictly associated with the differentiating vascular tissues. The association of the expression pattern with the provasculature is confirmed by the localization of the ZmPIN1 protein in the mature embryo axis. ZmPIN1 RNAs and proteins are always localized in the lateral developing primordia of the SAM, tassel, and ear and in the inner core of the meristems. During inflorescence development, ZmPIN1 is first localized in the cells corresponding to the central axis of the growing spikelet, and then it switches to the outer layers and central cells of the lower gluma. In the florets, ZmPIN1 is localized in the axis of the outgrowing organ. In the leaf primordia and leaves and in the male and female inflorescence, the ZmPIN1 proteins are localized in the vascular cell files on the basal membrane of the cells, suggesting an auxin flux directed basipetally. This is repeated in a whole strip of cells that encircles the inflorescence tip in the tassel. If we look at the inner tissues of the upper part of the tassel, we can see that ZmPIN1 is polarized in a way that suggests auxin fluxes spreading at 360° around a small group of cells (Fig. 9A ).
The complex polar patterns of ZmPIN1 might determine auxin distribution in the different maize tissues in synergy with other polarly distributed members of the PIN family, as in Arabidopsis. PIN proteins, together with other components, seem to form an auxin transport network that mediates local auxin distribution and triggers different cellular responses, according to the organ and developmental stage. Key members of this signaling network are the P glycoproteins (PGPs), the plant homologs of human multiple drug resistance proteins. They have been identified first in Arabidopsis and shown to mediate the transport of indole acetic acid (IAA) and IAA metabolites in HeLa cells, maize protoplasts, and in planta (Arabidopsis; Geisler et al., 2005 ). In particular, two members of the family, PGP1 and PGP19, have been functionally characterized and shown to determine phenotypic alterations in Arabidopsis, the main one being dwarfism (Geisler et al., 2003, 2005). Recently, the PGP1 orthologous gene has been cloned in maize (brachytic2 [br2]/ZmPGP1) and in Sorghum bicolor (dwarf3/SbPGP1) and shown to be responsible for IAA transport in the stem (Multani et al., 2003). The br2 mutant presents a dwarf phenotype with very short basal internodes, altered stem anatomy, and vascular tissue defects, and has been shown to have altered auxin transport. However, br2 inflorescences develop regularly and generate fertile progeny. Thus, for the future, it would be desirable to determine the possible interaction between maize PGP and PIN proteins, for example, studying the ZmPINs pattern in the br2 mutant.
In many tissues, distribution of maize proteins resembles the one observed for PIN1 in Arabidopsis. In general, the proteins are localized in provascular and vascular tissues and, in maize roots, their localization indicates that auxin is directed toward the root tip via the mature vascular tissues, as demonstrated for Arabidopsis (Benkova et al., 2003
The bif2 mutant presents abnormal branching of the female and male inflorescence (McSteen and Hake, 2001
Interestingly, whereas bif2 still shows vascular tissues with basally oriented PIN distribution, the group of cells carrying PIN just below the surface, observed in wild-type tassels and ears, was completely absent from the mutant. There are several possible explanations for this. First, BIF2 could be required to initiate this special population of cells. Their absence would subsequently lead to important changes in meristem function and organ initiation. It could also be that BIF2 has a more cellular role. It is noteworthy that we also frequently observed cells with upward-oriented PIN-labeled membranes in these cells. Because these orientations were not readily observed in the mutant, it could be, for instance, that BIF2 is required for orienting PIN in nonbasal orientations, much as PINOID in Arabidopsis (Friml et al., 2004
At the organ level, because the ZmPIN1 pattern is disrupted at the place of AM formation, it is possible that the lack of correct localization of ZmPIN1 in the provasculature indirectly causes the absence of BM, SAM, and/or SM formation and development. McSteen and Hake (2001)
Finally, possible redundancy of genes controlling branching in maize inflorescence, such as barren stalk1 (Ritter et al., 2002
Plant Material
The maize (Zea mays) B73 line was used for immunolocalization and in situ hybridization experiments. The maize mutant line bif2-2354 was obtained from the Maize Genetic Cooperation Stock Center (accessible online at http://www.maizegdb.org). This line was generated by ethylmethane sulfonate mutagenesis by M.G. Neuffer (Neuffer and Briggs, 1994
NCBI (http://www.ncbi.nlm.nih.gov), TIGR (http://www.tigr.org/), and MaizeGDB (http://www.maizegdb.org) were screened using the AtPIN1 (AT1G73590 for genomic DNA and AF089084 for cDNA) sequence as a query. Several maize expressed sequence tag (EST) sequences were collected and those that presented the higher similarity to AtPIN1 in the domain overlapping the anti-PIN1 peptide were chosen to design primers. A first primer combination (fwd, 5'-ATGATTACGGGGACGGACTTCTA-3' and rev, 5'-TCCAGACGAACATGTGGAGGTCCT-3') was used to amplify a genomic fragment of 1,050 bp at the 5' end of the gene. Sequencing revealed that the first primer combination used could amplify two different fragments. One of the two fragments contained an insertion of 44 bp at the end of the first exon. On this insertion, two forward primers (5'-GCAGGGCAAGGCGAACAAGTACGGCCAG-3' and 5'-CTCTCCCCGTGGTGAATGCGACGTCCG-3') were designed and used in combination with an oligo(dT)12–18 in RT-PCR amplifications. Sequencing of the amplified products allowed us to design new primers and obtain two distinct genomic clones. The primer combination (fwd, 5'-ATGATCACCGGCACGGACTTCTA-3' and rev, 5'-CGCTGTTGGCCTGCGGGAACGAGCAGC-3') amplified ZmPIN1a (2,770 bp), whereas the primer combination (fwd, 5'-CCACGCGTCCGGGATGGTCCAAGGAGAG-3' and rev, 5'-CTCAAGCCATCAAACTCCGGAGGTGAGC-3') amplified ZmPIN1b (3,300 bp). Cloning of the PCR amplification products was performed with the pCRII-TOPO TA-cloning kit (Invitrogen) and with the pGEM-T Easy vector systems (Promega). After sequencing on both strands, sequences were blasted as queries using BLASTn, BLASTx, and tBLASTx algorithms and proteic and nucleotidic similarities were determined. Sequences were edited and aligned using EditSeq and Megalign (Lasergene DNASTAR) software and grouped to form single consensus sequences using SeqMan software (Lasergene DNASTAR). Restriction maps were created using Web Map software (available at http://pga.mgh.harvard.edu/web_apps/web_map/start). GeneSeqer software was used to excise introns from genomic sequences before alignment and assembling.
PIN sequences from Arabidopsis (Arabidopsis thaliana), wheat (Triticum aestivum), and rice (Oryza sativa) were identified through a BLAST search of The Arabidopsis Information Resource (TAIR; http://www.arabidopsis.org) and TIGR (http://www.tigr.org) databases using AtPIN genes as query (Paponov et al., 2005
Genomic DNA was extracted from maize tissues, according to the Nucleon Phytopure extraction kit (Amersham). Total RNA was extracted from maize tissues (seedlings, young roots, shoot apexes, leaves, tassels, and ears) according to the RNeasy plant mini kit (Qiagen) and subjected to on-column DNase treatment. RT-PCR was performed with the SuperScript III reverse transcriptase kit (Invitrogen), according to the manufacturer's instructions. Two micrograms of total RNA were used as a template together with 1 µL oligo(dT)12–18 (25 µg/µL). ZmPIN1a (fwd, 5'-GTCAAGGAGGTCCGCATGGCCGTCGCC-3'; rev, 5'-CGCTGTTGGCCTGCGGGAACGAGCAGC-3') and ZmPIN1b (fwd, 5'-CTCTCCCCGTGGTGAATGCGACGTCCG-3'; rev, 5'-GAGCGTGATCGGCAGGGCGATGAGCAT-3') specific primer combinations were used for semiquantitative amplifications of the two transcripts. Each primer combination was used in multiplex amplification reactions together with Ubi (fwd, 5'-TAAGCTGCCGATGTGCCTGCGTCG-3') and Ubi (rev, 5'-CTGAAAGACAGAACATAATGAGCACAG-3'; Giulini et al., 2004
In situ hybridization experiments were carried out as described by Varotto et al. (2003)
Immunostaining was performed on wax-embedded (9:1; PEG400 distearate:1-hexadecanol 99%; Sigma) shoots, leaves, and inflorescences. Material was previously fixed in a 4% paraformaldehyde, 1x phosphate-buffered saline (PBS) solution for 1 h, under vacuum conditions at room temperature. Embedded tissues were cut with a Leica RM2135 microtome (Leica) and stained overnight with a 1:200 anti-PIN1 1x PBS, 1% bovine serum albumin solution. The next day, sections were washed twice for 10 min in 1x PBS and stained with the secondary antibody: anti-rabbit IgG conjugated with Alexa568 or Alexa488 (Molecular Probes) and/or with fluorescein isothiocyanate (Sigma) diluted 1:400 in 1x PBS for 1 h. Sections were washed twice for 10 min with 1x PBS and mounted with VECTASHIELD mounting medium (Vector Laboratories).
Immunostained slides were observed with a Leica TCS SP2 laser confocal microscope (Leica Microsystems). Images were collected frame by frame with the acousto-optical tunable filter using Ag-Kr and He-Ne laser lines 488 or 543/594 nm, respectively. Images were coded red for Alexa568; green for Alexa488 and fluorescein isothiocyanate labeling; and white/blue for autofluorescence. Histological analysis, in situ hybridization, and immunolabeled section images were acquired with a Leica DM4000B digital microscope, equipped with a Leica DC300F camera and Leica Image Manager 50 software (Leica Microsystems). Sequence data from this article have been deposited with the EMBL/GenBank data libraries under accession numbers DQ836239 and DQ836240 for ZmPIN1a and ZmPIN1b, respectively.
We thank V. Rossi for critical reading of the manuscript, C. Bonghi and E. Belles-Boix for helpful discussions, and T. Pengo for supporting experiments. Received March 6, 2006; accepted July 3, 2006.
1 This work was supported in part by the Università Italo-Francese (grants to N.C.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Serena Varotto (serena.varotto{at}unipd.it).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.106.080119 * Corresponding author; e-mail serena.varotto{at}unipd.it; fax 39–049–8272839.
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