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First published online January 18, 2008; 10.1104/pp.107.114108 Plant Physiology 146:1193-1206 (2008) © 2008 American Society of Plant Biologists
The Maize Viviparous8 Locus, Encoding a Putative ALTERED MERISTEM PROGRAM1-Like Peptidase, Regulates Abscisic Acid Accumulation and Coordinates Embryo and Endosperm Development1,[W]Plant Molecular and Cellular Biology Program, Horticultural Sciences Department, University of Florida, Gainesville, Florida 32611 (M.S., S.L., A.M.S., K.E.K., L.C.H., D.R.M.); Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi 464–8601, Japan (Y.S.); and RIKEN Plant Science Center, Yokohama, Kanagawa 230–0045, Japan (M.K., H.S.)
We describe a mutant of Zea mays isolated from a W22 inbred transposon population, widow's peak mutant1 (wpk1), with an altered pattern of anthocyanin synthesis and aleurone cell differentiation in endosperm. In addition, a failure of the developing mutant embryo to form leaf initials is associated with decreased expression of a subset of meristem regulatory genes that includes Abphyl1 and Td1. We show that the viviparous8 (vp8) mutant has a similar pleiotropic phenotype in the W22 inbred background in contrast to the viviparous embryo phenotype exhibited in the standard genetic background, and we confirmed that wpk1 is allelic to vp8. Further genetic analysis revealed that the standard vp8 stock contains an unlinked, partially dominant suppressor of the vp8 mutation that is not present in W22. Consistent with the early-onset viviparous phenotype of vp8, expression of several embryonic regulators, including LEC1/B3 domain transcription factors, was reduced in the mutant embryo. Moreover, reduced abscisic acid (ABA) content of vp8/wpk1 embryos was correlated with altered regulation of ABA biosynthesis, as well as ABA catabolic pathways. The ABA biosynthetic gene Vp14 was down-regulated in the nonsuppressed background, whereas the ZmABA8'oxA1a ABA 8'-hydroxylase gene was strongly up-regulated in both genetic backgrounds. Molecular analysis revealed that Vp8 encodes a putative peptidase closely related to Arabidopsis thaliana ALTERED MERISTEM PROGRAM1. Because the Vp8 regulates meristem development as well as seed maturation processes, including ABA accumulation, we propose that VP8 is required for synthesis of an unidentified signal that integrates meristem and embryo formation in seeds.
In flowering plants, seed development begins with double fertilization generating a diploid zygote that undergoes embryogenesis and a triploid central cell that develops as endosperm. As organogenesis nears completion, the embryo and endosperm enter a maturation phase characterized by developmental arrest and acquisition of dormancy.
Genetic studies in Arabidopsis (Arabidopsis thaliana) and maize (Zea mays) have identified two classes of transcription factors that are essential for seed maturation and dormancy processes. The first class of genes, exemplified by Arabidopsis LEC1 and L1L, encode HAP3-related transcription factors (Lotan et al., 1998
Control of maturation by the B3 transcription factor network is further determined by interactions with hormone signaling pathways. For example, the ABI3/VP1 transcription factor has a unique capacity to interact with abscisic acid (ABA) signaling conferred by physical interaction with ABI5 (Hobo et al., 1999
Endosperm differentiation and maturation proceed in parallel with embryo development (for review, see Olsen, 2001 Here we describe genetic and molecular analysis of the maize vp8 mutant in embryo and endosperm development. We show that novel widow's peak1 (wpk1) mutations that alter the pattern of aleurone differentiation in the adgerminal region of the endosperm are allelic to vp8. Genetic analyses reveal that the vp8 phenotype is strongly conditioned by genetic background in maize due to action of an unlinked semidominant suppressor locus. Our results suggest that the pleiotropic effects of the vp8 mutation are mediated through regulation of specific meristem and embryonic regulatory genes and by regulation of genes controlling ABA biosynthesis and turnover in the developing seed. Finally, we cloned the Vp8 gene and show that it encodes a putative membrane peptidase closely related to Arabidopsis ALTERED MERISTEM PROGRAM1 (AMP1).
Isolation of wpk1 Mutants
To search for new mutations that affect differentiation of aleurone in maize, we screened the UniformMu inbred transposon-tagging population (McCarty et al., 2005
Aleurone Development in the wpk1 Mutant Taking advantage of the genetic background of the UniformMu population, we examined the pattern of aleurone differentiation marked by anthocyanin accumulation in the wpk1 mutant seeds. In wild-type kernels, pigmentation of aleurone was typically visible by 14 DAP in our spring field conditions, initiating in a ring of aleurone cells (Fig. 2A ). In the wpk1 mutant, the onset of anthocyanin accumulation was delayed by up to several days and typically failed to occur at all in aleurone cells surrounding the embryo on the adgerminal face of the kernel. Within several days following the onset of pigment accumulation, the crown and adgerminal regions of wild-type kernels were completely pigmented, whereas the lower portion of the abgerminal aleurone remained colorless (Fig. 2B). In contrast to wild type, pigmentation of the abgerminal aleurone of wpk1 mutant seed was frequently enhanced relative to wild type, forming irregular patches of pigmented aleurone (Fig. 2C). This result suggested that Wpk1 regulation of anthocyanin accumulation is region specific.
Maize Cr4, which encodes a plasma membrane receptor kinase, is a positive regulator of abgerminal aleurone differentiation in endosperm (Becraft et al., 1996  ). To test whether Cr4 and Wpk1 genetically interact in aleurone differentiation, we constructed cr4 wpk1 double-mutant seeds to examine pigmentation and patterning of the aleurone (Supplemental Fig. S3). The double-mutant seeds exhibited anthocyanin deficiencies in both adgerminal and abgerminal regions. The aleurone phenotype was consistent with an additive superposition of the cr4 and wpk1 single-mutant patterns of anthocyanin accumulation in the aleurone. This result implies that these two genes most likely function independently in aleurone development. The opposite polarities of the vp8 and cr4 phenotypes with respect to the adgerminal/abgerminal axis of the endosperm suggest that development of adgerminal and abgerminal domains may be separately regulated (Becraft and Asuncion-Crabb, 2000). In addition to the distinctive pattern of anthocyanin pigmentation, the size and morphology of aleurone cells was strongly affected in wpk1 mutant seeds. The wpk1 mutant aleurone cells in the abgerminal, as well as adgerminal, region were markedly elongated in the anticlinal direction, but not in the periclinal plane (Fig. 2, D–G). Measurement of cell lengths of 15 cells shown in Figure 2E indicated an average length 1.6-fold greater than comparable aleurone cells in wild-type kernels. This result indicated that the Wpk1 gene suppresses anticlinal cell expansion of aleurone cells of the endosperm. Whereas cell elongation was most pronounced in the anthocyanin-deficient cells proximal to the embryo, slight elongation of aleurone cells was detected throughout the aleurone of wpk1 seeds, suggesting that cell size and anthocyanin accumulation patterns may be independently regulated by the Wpk1 gene.
Because the wpk1 mutation significantly altered organization of the embryonic SAM, we determined whether expression of genes that are known to regulate SAM formation in grasses was affected during mid-to-late embryo development (12, 14, and 16 DAP) when wild-type W22 embryos continue to produce new leaf primordia (Supplemental Fig. S2). Interestingly, the wpk1 mutant affected expression of a subset, but not all, of SAM markers (Fig. 3
). Expression of Abnormal phyllotaxy1 (Abphyl1; Asakura et al., 2003
The wpk1 Mutant Is Allelic to vp8
In a parallel study of the vp8 mutant (Robertson, 1955
To understand the basis for the altered expression of vp8-R in the SC and W22 backgrounds, we performed a characterization of embryo and aleurone development in vp8-R (SC) and vp8-R (W22) seeds and compared their phenotypes to vp8-umu1. In contrast to the vp8-R and vp8-umu1 mutations in the W22 background, vp8-R (SC) mutant embryos were viable if rescued prior to desiccation as previously reported (Evans and Poethig, 1997 ; Supplemental Fig. S3). The mutant was capable of forming a well-organized SAM and leaf initials with comparable size of the cells in the developing embryo (Fig. 4, C and D). The aleurone layer of vp8-R (SC) kernels did not show marked differences from wild type (Fig. 4, E and F). Whereas the absence of C1 and R1 alleles required for anthocyanin biosynthesis prevented evaluation of pigmentation patterns in the SC background, mutant aleurone cells were elongated only slightly compared to wild type (1.15-fold longer in the anticlinal direction compared to the wild-type control). Furthermore, unlike vp8-umu1, we did not detect increased early seed abortion or less than expected frequencies of viviparous seeds on the self-pollinated ears (Supplemental Table S2). To compare meristem function in the SC and W22 backgrounds, expression profiles of meristem marker genes in developing vp8-R (SC) and vp8-R (W22) embryos were determined by reverse transcription (RT)-PCR (Fig. 4G). In the SC background, all of the meristem markers, except Abphyl1, showed comparable expression profiles in wild-type and mutant embryos. In marked contrast to vp8-R (W22) and vp8-umu1 embryos, vp8-R (SC) showed no evidence of altered expression of Td1. Whereas Abphyl1 expression was reduced in both the W22 and SC backgrounds, the effect was more pronounced in the W22 background. The comparatively subtle changes in gene expression of meristem-related genes in the SC background were consistent with the observation that the vp8-R (SC) mutant embryo was able to develop a functional SAM. Similar to vp8-umu1, Fea2 and ZmPLA1 genes were unaffected by vp8-R in both the W22 and SC backgrounds. Expression of Rs2 and Kn1 genes was slightly decreased in vp8-R (W22) embryos compared to wild type. These subtle differences are most likely due to environmental effects on embryo development because we detected similar differences in the vp8-umu1 between two seasons (Fig. 3; Supplemental Fig. S4). Overall, these results indicated that genetic background differences between W22 and SC had a much more profound effect on the vp8 phenotype than allele differences.
To identify genetic factors that interact with the vp8 mutation in W22 and SC genetic backgrounds, we analyzed the seed and seedling phenotypes of F1 plants generated by reciprocal crosses between vp8-R (SC) and vp8-umu1. All of the heteroallelic vp8 mutant seed from crosses made in either direction developed embryos comparable in size to wild type (Table I ; Supplemental Fig. S5). The characteristic wpk1 phenotypes, including severe defective embryo and patterned anthocyanin deficiency, were not observed in the F1 seed. These results indicated that the SC background is able to suppress the wpk1 defective embryo sufficiently to produce a well-developed embryo that is in some cases viviparous. In spring (warm) as well as fall (cool) field environments, viviparous embryos were frequently observed in the F1 seeds derived from crosses between vp8-R (SC) females and vp8-umu1 male parents, whereas F1 seed from the reciprocal cross predominantly had an intermediate phenotype with near full-size embryos that were weakly viviparous. The qualitative difference in the phenotypes of reciprocal F1 hybrid seed suggested that either maternal factors or gametophytic transmission affected vp8 function in the developing seed. In this respect, it is noteworthy that, in some of the crosses involving vp8-R (W22) made in either direction, mutant seed was recovered at a lower than expected frequency consistent with Vp8 having a function in both male and female gametophytes (Table I).
To determine whether embryos with strong and intermediate viviparous phenotypes were viable and capable of growing into seedlings, we rescued these mutant embryos and placed them in sterile culture. Unlike vp8-umu1, the viviparous vp8-R (SC) mutants and heteroallelic F1 mutant embryos developed shoots at >90% frequency (Supplemental Fig. S6). The results of reciprocal crosses indicated that one or more dominant genetic factors in the SC background partially suppress the severe developmental defects caused by the vp8 mutation in W22. To estimate the number of genetic loci involved in suppression of vp8 in the SC background, we analyzed the phenotypes of F2 seeds generated from the heteroallelic F1 seeds as well as of F2 seeds from backcrosses of vp8-R (SC) with W22 (Table II ). The mutant F2 seeds were grouped in three phenotype classes: strongly viviparous, intermediate, and wpk-like, respectively. Within the mutant class, the viviparous plus intermediate and wpk-like embryos occurred in a ratio that was consistent with segregation of a single, unlinked partially dominant suppressor. The SC and W22 inbreds are evidently homozygous for dominant and recessive alleles of the suppressor, respectively.
Altered Regulation of ABA Synthesis and Turnover in the vp8 Mutant
The vp8-R (SC) genotype has been previously reported to have moderately reduced levels of ABA in the developing embryo (Neill et al., 1986
To examine the potential role of hormone biosynthesis in the complex phenotype of vp8 mutants, we analyzed levels of three key plant hormones, ABA, auxin, and cytokinin, in developing embryo and endosperm tissues of wild-type and mutant seeds. Consistent with the previous report by Neill et al. (1986)
To gain insight into how ABA accumulation is regulated by Vp8, we analyzed expression of key genes, Vp14 and ZmABA8'oxA1a, that are implicated in control of ABA biosynthesis and degradation, respectively. The Vp14 gene encodes the major 9-cis-carotenoid dioxygenase expressed during maize embryo development (Tan et al., 1997 ), and ZmABA8'oxA1a is an ortholog of the ABA 8'-hydroxylases (Kushiro et al., 2004; Saito et al., 2004; Millar et al., 2006; Okamoto et al., 2006; Yang and Choi, 2006; Yang and Zeevaart, 2006; Saika et al., 2007) that catalyzes the first step in catabolism of ABA. As shown in Figure 5B, Vp14 expression was significantly lower in developing vp8-umu1 (W22) embryos, whereas expression of Vp14 in vp8-R (SC) embryos was similar to wild type. In contrast, ZmABA8'oxA1a expression was markedly elevated in vp8 mutant embryos in both the SC and W22 genetic backgrounds. These results indicate that the severe ABA deficiency evident in the W22 background correlates with simultaneous down-regulation of ABA biosynthesis and up-regulation of ABA catabolism pathways, whereas the moderate ABA deficiency conditioned by vp8 in the SC background is primarily due to elevated ABA catabolism. A key implication is that the dominant suppressor in the SC background restores regulation of ABA biosynthesis, but not repression of ABA catabolism. These results are consistent with the independent evidence that both ABA biosynthesis and turnover contribute to regulation of seed development and germination (for review, see Nambara and Marion-Poll, 2005).
Although the reduced ABA accumulation in vp8 mutant embryos is consistent with the viviparous phenotype, ABA deficiency alone seems unlikely to account for the pleiotropic phenotypes of vp8 in embryo, aleurone, and vegetative organs. To better understand the complex embryo phenotype, we analyzed expression of the LEC1-related factors and B3 domain transcription factors that regulate embryogenesis and maturation. In Arabidopsis, loss-of-function mutations at four loci, lec1, lec2, fus3, and abi3, prevent embryo maturation and induce a potential for viviparous seed development. The ABI3 gene and its maize ortholog, Vp1, are required for ABA-regulated gene expression late in seed development, whereas lec1, lec2, and fus3 genes affect earlier stages of seed development. Because aspects of the vp8 phenotype are manifest at early stages of seed development, we considered the possibility that Vp8 may also interact with the early-acting regulators of embryogenesis in maize.
To develop RT-PCR assays for expression of the maize embryo pathway, we searched available genome and EST databases to identify maize orthologs of the Arabidopsis HAP3 and B3 transcription factor genes. We identified three homologs of the Arabidopsis LEC1 and L1L HAP3-related genes (ZmLEC1, ZmL1La, and ZmL1Lb, respectively) based on the similarity of the HAP3 domains (M. Suzuki, unpublished data). A LEC1 ortholog identical to ZmL1La has been described previously (Zhang et al., 2002 As shown in Figure 6 , expression of ZmLEC1, ZmL1La, ZmL1Lb, ZmFUS3, and Vp1 was reduced in vp8 mutant embryos in both W22 and SC backgrounds. Whereas all five genes showed quantitatively lower expression in vp8 embryos late in development (18 and 20 DAP), ZmL1Lb expression, which was not detected in vp8 embryos after 18 DAP, showed the most striking qualitative difference between wild type and vp8 common to both backgrounds. Interestingly, the ZmL1La and ZmL1Lb genes were differentially expressed in the wild-type SC and W22 backgrounds. ZmL1La expression was relatively high compared to ZmL1Lb throughout development in SC embryos, whereas ZmL1Lb and ZmL1La were expressed at similar levels in W22 embryos. Hence, among the embryogenesis regulators tested, only ZmL1Lb and ZmL1La exhibited expression differences that correlated with partial suppression of the vp8 phenotype. In any case, because vp8 embryos in the suppressed background are fully formed, the qualitative differences in expression of the embryo pathway genes are likely to be caused by specific action of the Vp8 gene, but not by nonspecific effects due to gross morphological defects in embryo formation. This interpretation is further supported by the observation that expression of ZmL1Lb, in contrast to the other embryonic regulators, was clearly reduced in the vp8-R (SC) mutant at 18 DAP under greenhouse conditions. Although the viviparous phenotype of greenhouse-grown vp8-R (SC) embryos is barely discerned at 18 DAP, embryo genotypes were confirmed by subsequent RT-PCR analysis for the presence of detectable Vp8 mRNA (see Fig. 7B ).
Cloning of the Vp8 Gene by Transposon Tagging Performed in Silico
Our screen of the UniformMu population (McCarty et al., 2005
To clone the vp8 locus, we performed MuTAIL-PCR (Settles et al., 2004
We performed RT-PCR to analyze expression of Vp8 in wild-type and vp8 mutant embryos (Fig. 7B). A Vp8 transcript was detected in the W22 inbred but not in vp8-umu1 and vp8-umu2 mutants, indicating that the transposon insertions disrupted transcription or mRNA stability. Although the molecular lesion in the vp8-R allele was not determined, the reference allele was also null for mRNA expression based on RT-PCR. In the developing seed of wild type, expression of the Vp8 gene was markedly higher in the embryo than in endosperm on a total RNA basis (Fig. 7C). Vp8 expression was detected as early as in 6-DAP developing seed, as well as in various vegetative tissues at lower levels (Fig. 7D), consistent with AMP1 gene expression in Arabidopsis (Helliwell et al., 2001
To determine the complete sequence of the VP8 protein, we isolated and sequenced a full-length cDNA of Vp8 mRNA by RT-PCR using RNA prepared from W22 developing embryos. We designed primers based on maize genome survey sequences that contained the predicted 5' and 3' untranslated regions of the gene. The cDNA sequence predicted a protein of 714 amino acids that aligns with two membrane-localized glutamate carboxypeptidases from human (Israeli et al., 1993
Our results show that maize Vp8 encodes a putative membrane-localized peptidase that is closely related to Arabidopsis AMP1. Loss of Vp8 function causes either lethality or precocious germination of the developing embryo, depending on the genetic background. The vp8 mutant is highly pleiotropic in the W22 inbred, indicating that the gene is essential for a wide range of developmental processes in maize. In the developing embryo, the Vp8 gene is required for expression of LEC1/B3 embryonic regulators, as well as for genes that regulate ABA synthesis and turnover. Vp8 effects on SAM organization are associated with reduced expression of a specific subset of meristem-related genes. Finally, we have identified a partially dominant suppressor that genetically interacts with vp8 in regulation of plant development in maize.
Although it remains to be determined whether maize Vp8 is capable of complementing the Arabidopsis amp1 mutant, the similarities in the pleiotropic phenotypes of the amp1 and vp8-R (SC) mutants, as well as in the protein structures of AMP1 and VP8, suggest that these genes are likely orthologs. Whereas the precise mechanisms of SAM development and leaf differentiation are thought to be distinct in Arabidopsis and maize (Scanlon, 2000
Although amp1 and vp8 have analogous phenotypes, the mutants differ in their reported effects on hormone synthesis. In Arabidopsis, amp1 mutant seedlings are reported to have elevated cytokinin levels compared to wild type (Chaudhury et al., 1993
Among the embryonic regulatory genes we analyzed, ZmL1Lb shows the earliest detectable difference in the expression in vp8 mutant embryos prior to discernible vivipary, thus suggesting that ZmL1Lb may be a primary target of unidentified factors derived from Vp8 function. In Arabidopsis, LEC1 has been proposed to be an upstream activator for FUS3 and ABI3 B3 domain genes (Kagaya et al., 2005
The down-regulation of LEC1/B3 genes in the vp8 may account for regulation of ABA accumulation as well as affect maturation-related gene expression. FUS3 has been shown to regulate ABA accumulation in developing seeds of Arabidopsis (Nambara et al., 2000
Whereas vp8 mutation alters development and gene expression in meristem as well as nonmeristem tissues of the embryo, it is not yet clear whether the dual effects are mediated by the same or distinct independent mechanisms. One possibility is that AMP1/Vp8 establishes a regulatory field that is interpreted locally to produce diverse responses in different tissues. In the meristem of Arabidopsis, AMP1 function is implicated in cytokinin signaling (Chaudhury et al., 1993
The isolation of vp8 alleles in the nonsuppressed W22 inbred background proved crucial to uncovering the unexpectedly broad and essential role of Vp8 in embryo and endosperm development. One of the notable findings is that Vp8 is likely required for normal cell division and expansion processes in the developing embryo as well as in the aleurone. Although Arabidopsis AMP1 is expressed throughout the tissues, expression of this gene is relatively higher in rapidly dividing tissues such as in shoot and root meristems (Schmid et al., 2005
Our finding of a suppressor, together with the highly pleiotropic nature of the vp8 phenotype, suggests that a search for other interacting genes may be fruitful. Other genes that interact with Vp8 function in cereal seed development have so far not been identified. Whereas the maize terminal ear1 (te1), rice pla1, and pla2 mutants have accelerated leaf formation similar to that seen in vp8-R (SC) plants during vegetative development, no differences in seed development have been described in these mutants (Itoh et al., 1998
The discovery that the Vp8 gene encodes a putative peptidase, together with the irregular pattern of aleurone pigmentation, is consistent with diffusion of a nonautonomous signal derived from Vp8 activity. Interestingly, Vp8 is expressed at significantly lower levels in endosperm than in embryo, suggesting the possibility that the abnormal endosperm development might be caused by embryo-derived diffusible signals. Several classes of plant peptides have been identified in signaling (for review, see Boller, 2005
Plant Material The vp8-R stock was obtained from the Maize Genetics Cooperation Stock Center. The vp8-R (W22) material used in this study was established by backcrossing the original vp8-R with the W22 inbred line five times. For the vp8-umu1, vp8-umu2, vp8-umu3, and vp8-umu4 alleles, the complementation tests were performed by generating at least five independent crosses between vp8-R and each of the vp8-umu heterozygous mutants.
The vp8-umu1 and vp8-R (SC) heterozygous plants were self-pollinated and the resulting developing seeds were used for embryo rescue experiments. The heteroallelic F1 seeds were generated by crosses of vp8-umu1 (W22) and vp8-R (SC). Embryos excised from 20- or 22-DAP seeds were placed on culture medium, as previously described (Suzuki et al., 2006
The MuTAIL library construction and processing and assembly of the sequences were described previously (Settles et al., 2004
Total RNA was prepared from maize (Zea mays) embryos, DNaseI treated, and purified using the RNeasy kit (Qiagen). Total RNA from maize endosperm was extracted as previously described (McCarty, 1986
Quantification of hormones was performed as described (Nakagawa et al., 2005 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number EU401893.
The following materials are available in the online version of this article.
We thank the ICBR at the University of Florida for DNA sequencing. We also thank the Maize Genetics Cooperation Stock Center for providing vp8-R seed stock and Dr. Philip Stinard at the Center for providing pedigree information regarding this mutant allele. Received November 27, 2007; accepted January 12, 2008; published January 18, 2008.
1 This work was supported by the National Science Foundation (grant nos. 0077676 and 0322005).  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: Masaharu Suzuki (masaharu{at}ufl.edu).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.107.114108 * Corresponding author; e-mail masaharu{at}ufl.edu.
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ABSTRACT
RESULTS
2 tests and P values were calculated for a model that assumed that normal and all mutant classes (viviparous + intermediate + wpk) segregate 3:1.
