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The SHOOTLESS2 and SHOOTLESS1 Genes Are Involved in Both Initiation and Maintenance of the Shoot Apical Meristem Through Regulating the Number of Indeterminate Cells
Namiko Satoha, Jun-Ichi Itoha, and Yasuo Nagatoaa Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo 113-8657, Japan
Corresponding author: Yasuo Nagato, University of Tokyo, Tokyo 113-8657, Japan., anagato{at}mail.ecc.u-tokyo.ac.jp (E-mail)
Communicating editor: V. SUNDARESAN
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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To characterize the SHL2 and SHL1 genes in detail, we analyzed three strains carrying weak alleles of SHL2, shl2-6, shl2-7, and shl2-8, and one weak allele of SHL1, shl1-3. In contrast to strong alleles, which result in lack of shoot meristem, strains bearing these weak alleles formed shoot meristem frequently during embryogenesis. In shl2-6 and shl2-7 mutants, the meristem was lost during seed development. Only the shl2-8 mutant could survive after germination, but it showed abnormal initiation pattern and morphology of leaves. In strains bearing the weak alleles, the shoot meristem was composed of a small number of indeterminate cells and ultimately converted into leaf primordium. The shl1-3 mutant showed phenotypes similar to those of shl2-8. Thus SHL2 and SHL1 are required for both initiation and maintenance of shoot meristem. In shl2 mutants, there was a positive correlation between the size of the expression domain of OSH1 representing the number of indeterminate cells, the frequency of shoot meristem initiation, and the duration of meristem survival. Thus the shoot meristem will not initiate in an "all-or-nothing" fashion, but is formed in various degrees depending on the strength of the alleles. Double-mutant analyses indicate that SHL2 functions upstream of SHO to establish proper organization of the shoot meristem.
THE shoot system is constructed throughout the plant life cycle by the continuous activity of small groups of cells called shoot apical meristems (SAMs). The SAM originates during embryogenesis and is later responsible for generating the aboveground organs of the plant. Thus, understanding the developmental events that determine the aboveground architecture requires detailed examination of the SAM. The SAM can be thought of as having two fundamental functions: self-perpetuation and the formation of lateral organs (for review see 
Several key genes that play important roles in the above functions of the SAM have been studied in Arabidopsis, maize, and rice. As for the maintenance of the Arabidopsis SAM, SHOOT MERISTEMLESS (STM) functions to keep central meristem cells indeterminate (
In monocots, which have distinct organization of embryos and shoots compared to dicots, the SAM development is poorly understood. In rice, recessive mutations in at least four loci cause loss of the SAM without affecting radicle differentiation (
Maintenance of the SAM is balanced with the process of organogenesis. In Arabidopsis, STM and CLV genes competitively regulate the balance between undifferentiated cells and lateral organs (
In spite of these studies, the mechanisms for SAM maintenance have not been well understood. In rice, at least four SHOOTLESS (SHL) genes are indispensable for SAM initiation (
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plant materials:
Mutants used in this study are summarized in Table 1. We identified three weak recessive alleles of the SHL2 locus on chromosome 1 in rice (Oryza sativa L.), shl2-6, shl2-7, and shl2-8, from M2 populations mutagenized with N-methyl-N-nitrosourea (MNU). The shl2-6 and shl2-8 were derived from cv. Taichung 65, and shl2-7 was derived from cv. Kinmaze. We also identified a strong recessive allele, shl2-9. Although the strong alleles (shl2-1–shl2-5) thus far reported (
25% and by the segregation value in F2 progeny.
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Since the seedlings of shl2 weak alleles were similar to those of sho mutants (
Growth conditions:
As the mutant seedlings of shl2-6, shl2-7, shl2-8, and shl1-3 became etiolated when grown in soil, plants were grown aseptically on MS medium (
Preparation of plastic sections:
Developing seeds and seedlings were fixed in FAA (formalin:glacial acetic acid:70% ethanol; 1:1:18) and dehydrated in a graded ethanol series. They were embedded in a resin, Technovit 7100 (Kurzer, Germany), polymerized at 45°, and sectioned at 3–5 µm thick. Sections were stained with toluidine blue and observed with a light microscope.
Scanning electron microscopy:
Shoot apices were fixed with 2.5% glutaraldehyde in 0.1 M sodium phosphate buffer (pH 7.2) for about 16 hr at 4°. After rinsing with 0.1 M sodium phosphate buffer (pH 7.2), they were postfixed in 1% osmium tetroxide for 3 hr at 4° and rinsed with buffer. Then samples were dehydrated in a graded ethanol series, and 100% ethanol was replaced with 3-methyl-butyl-acetate. Samples were critical-point dried, sputter coated with platinum, and observed with a scanning electron microscope (model S-4000, Hitachi, Tokyo) at an accelerating voltage of 10 kV.
In situ hybridization:
Embryos and shoot apices were fixed in 4% paraformaldehyde and 0.25% glutaraldehyde in 0.1 M sodium phosphate buffer. Then they were dehydrated in a graded ethanol series, replaced with xylene, and embedded in Paraplast Plus (Oxford Labware, St. Louis). Microtome sections (8 µm thick) were applied onto glass slides coated with Vectabond (Vector Laboratories, Burlingame, CA). Digoxygenin-labeled antisense probes were prepared from the coding regions of histone H4 and OSH1 deprived of their poly(A) ends. In situ hybridization and immunological detection were carried out by the methods of
To estimate the number of cells expressing OSH1, we stained the nuclei of the embryo sections used for in situ hybridization with 4',6-diamidino-2-phenylindole, and we counted the number of nuclei in the OSH1-expression domain. We used five embryos of the wild type and each mutant just before SAM initiation [3 days after pollination (DAP) in the wild type and 5 DAP in mutants].
Induction of calli and shoot regeneration:
Detection of mature mutant seeds under a dissecting microscope was based on the absence of the coleoptile and confirmed by a lack of shoot germination 2 days after imbibition. The seeds were sterilized with 2% sodium hypochlorite for 30 min and washed with sterilized water. For the induction of calli, they were inoculated onto N6 medium (5 mm in diameter, they were transferred onto regeneration medium containing MS salt and vitamins (
| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Since the shl2 alleles (shl2-1–shl2-5) thus far reported (
Embryo development in shl2 mutants:
Embryo phenotype:
The developmental course of embryos was examined in wild type and in strong (shl2-3) and weak (shl2-6, -7, and -8) mutants (Fig 1). In the wild-type embryo, the globular stage lasts until 3 DAP. At 4 DAP, the coleoptile, shoot, and radicle meristems are first observed, and the first leaf primordium is apparent at 5 DAP (Fig 1A). In embryos of shl2 mutants, the protrusion of the coleoptile did not occur, and no organs were formed except for scutellum and radicle (Fig 1, B–E). Up to 5 DAP, embryo phenotypes of strong (shl2-3) and weak (shl2-6–shl2-8) alleles were indistinguishable from each other. At 6–7 DAP, although no further morphological changes occurred in shl2-3 embryos (Fig 1G), shl2-6–shl2-8 mutants frequently initiated a SAM, epiblast, and first leaf primordium, but lacked a coleoptile (Fig 1, H–J). The frequencies of SAM initiation in shl2-6, shl2-7, and shl2-8 were 55, 77, and 93%, respectively. In shl2-6 embryos, however, the SAM disappeared after producing one or two leaf primordia, resulting in a SAM-less mature embryo (Fig 1M; Table 2). Also, in the weaker allele, shl2-7, the SAM was lost in most embryos after forming two or three leaf primordia (Fig 1N). In these two alleles, the SAM seemed to be consumed during the production of leaf primordia. In contrast, a SAM survived in more than half of the mature shl2-8 embryos, which had three leaf primordia (Fig 1O; Table 2). The SAM of shl2-8 was maintained for 1–4 weeks after germination. Thus, shl2-8 is the weakest allele, judging from the embryo phenotype (frequencies of SAM initiation and of mature embryos with SAM). These results show that the SHL2 gene is essential for maintaining the SAM.
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Interestingly, the first leaf in shl2-6–shl2-8 mutants was initiated at the normal position, but was thicker than that in the wild type, and its epidermis was composed of palisade-shaped cells, which are characteristic of scutellar epithelium (data not shown).
OSH1 expression:
To examine the organization of the SAM in shl2 embryos, we examined the expression of OSH1, a rice counterpart gene of the maize homeobox gene kn1, which marks indeterminate cells in the SAM (
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Interestingly, the expression domain of OSH1 (the number of indeterminate cells) seemed to be positively correlated with the frequency of SAM initiation. Then we counted the number of cells expressing OSH1 of the above mutants and the strongest allele shl2-9 using embryos just before SAM formation (Fig 3). As for shl2-3 and shl2-9, we used 5-DAP embryos. Among the shl2 mutant alleles, the number of cells expressing OSH1 is largest in shl2-8, smallest in the strong allele shl2-9, and intermediate in shl2-6 and shl2-7. It is clear that the number of cells is positively correlated with the frequency of SAM initiation (Fig 3). On the basis of this correlation, we can estimate a threshold value of the number of cells expressing OSH1 (indeterminate cells) required for initiating SAM. Since 106 cells expressed OSH1 in the wild-type embryo and 73 cells expressed OSH1 in the shl2-8 embryo, 80 or more indeterminate cells expressing OSH1 are needed for initiating normal SAM. The shl2-6 embryo expressed OSH1 in 38 cells on average and initiates SAM, but the shl2-3 embryo expressed OSH1 in 25 cells and failed to initiate SAM. Thus, SAM is formed but ill organized if 30–80 cells are recruited for expressing OSH1. If only 
30 cells express OSH1, SAM is not formed. In addition, the duration of SAM maintenance (Table 2) is also correlated with the number of cells expressing OSH1 among weak alleles. Accordingly, the domain size of indeterminate cells regulates the initiation and subsequent maintenance of SAM.
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Plant phenotypes of weak shl2 mutants:
Strains bearing any of the three weak shl2 alleles were able to germinate. However, shl2-6 and shl2-7 seedlings developed a few malformed leaves that were already present in the embryo and then aborted. In these seedlings, a SAM was not observed. In contrast, a considerable number of shl2-8 seedlings survived for a few weeks, but developed into abnormal plants. Some shl2-8 plants grew longer, but none survived >2 months. Since shl2-8 seedlings were relatively vigorous and showed a variety of interesting phenotypes, we examined the shoots of shl2-8 in detail.
Early vegetative phase: Within 1 week after germination, shl2-8 seedlings were characterized by the rapid production of small narrow leaves with irregular phyllotaxy (Fig 4). The mean plastochron was <2 days, about half that of the wild type, and the phyllotaxy was quite irregular (Fig 4B and Fig C). The leaf morphology varied between seedlings; thread-like leaves and relatively wide leaves were observed, although these were much narrower than wild-type leaves (Fig 4B and Fig C). The narrow thread-like leaves had one vascular bundle in the center and their primordia were very narrow due to the defect in recruiting enough founder cells (Fig 4C). Relatively wide leaves seemed to be derived from a relatively large number of founder cells (Fig 4C).
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In many shl2-8 seedlings, a SAM was not visible at the base of the most recent leaf primordium. In some cases, a trichome was formed at the tip of a dome-like structure, which was in the position normally occupied by the SAM. In other cases, a leaf primordium was present at the position of SAM (Fig 4D). Considering the fact that more than half of shl2-8 seedlings arrested their growth at 1 week after germination (Table 2), the above observations imply that the SAM of shl2-8 seedlings disappears due to its conversion into a leaf primordium. The SAM of shl2-8 surviving seedlings was abnormally shaped. In general, the SAM was wider in the mutant than in the wild type, but its height was nearly half that of the wild type, resulting in a flat shape (Fig 4F and Fig G).
To elucidate how cells were organized in the misshaped SAM, we examined the expression pattern of OSH1 (Fig 4, E–G). In the SAMs of surviving shl2-8 seedlings, OSH1 was expressed in a slightly smaller region than in the wild-type SAM (Fig 4F and Fig G), although several SAMs showed apparently normal OSH1 expression. In many cases, the downregulation of OSH1 expression occurred in the peripheral and rib zones (Fig 4F and Fig G). These results indicate that at the seedling stage, the proportion of indeterminate cells was reduced in the shl2-8 SAM and may be the cause of rapid and irregular initiation of leaf primordia.
To understand the rapid leaf production in shl2-8 mutants, we examined the expression of the histone H4 gene, which is expressed specifically in the S phase of the cell cycle. In the wild-type SAM at 1 week after germination, hybridization signals were detected in no more than two cells of the peripheral zone in the median longitudinal plane (Fig 5A). However, cells with hybridization signals were more frequent in the SAM of shl2-8 seedlings than in the wild type (Fig 5B and Fig C), indicating that shl2-8 mutants had accelerated cell divisions in the SAM. In addition, the cells expressing histone H4 were not restricted to the peripheral zone (where cell division activity was relatively high in the wild-type SAM), but were also frequently detected in the central zone (Fig 5B and Fig C). These results indicate that the SAMs of shl2-8 mutants are abnormally organized and are defective in the spatial regulation of cell divisions.
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A variety of leaf abnormalities were detected in shl2-8 seedlings (Fig 6). Relatively wide leaves often split into two or three at the tip (Fig 6C). Many leaves showed aberrant histology: the adaxial epidermal cells in the basal region of the leaf underwent extra anticlinal divisions whereas at the tip they became enlarged. Other histological abnormalities were also observed (Fig 6D and Fig E). The thread-like leaves showed normal histology (Fig 6F). Thus shl2-8 affects both the morphogenesis and the initiation pattern (phyllotaxy and plastochron) of leaves, as well as the leaf histology.
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Late vegetative phase: shl2-8 plants that survived past 1 week after germination were different from younger seedlings in several traits (Fig 7). In the surviving plants at 2–3 weeks after germination, all the leaves were thread-like, and the phyllotaxy was mostly distichous (Fig 7A and Fig B). The leaves at this stage showed normal histology (Fig 6G). Subsequently, the leaf size was progressively reduced, and by 2 months after germination, no more leaves were formed, and growth terminated. As observed in the early phase, a trichome was often formed at the tip of the apical dome, suggesting that the SAM was partially converted into a trichome (Fig 7C and Fig E). In other cases, a leaf primordium was observed in the position of the SAM (Fig 7B and Fig F), suggesting that SAM was converted into a leaf primordium.
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In shl2-8 mutants at this stage, OSH1 was expressed in a narrow region of the flat SAM (Fig 7D and Fig E). In the wild-type SAM, expression was downregulated in the L1 layer and in leaf primordia. In shl2-8, in addition to these regions, downregulation was also observed in a considerably wide region of the SAM (Fig 7D). When the apex showed leaf identity, two patterns of OSH1 expression were observed. When a trichome was formed from the apical L1 layer, OSH1 was expressed in a small internal region of the SAM (Fig 7E). In another case, OSH1 was not expressed, and the whole apex was converted into a leaf (Fig 7F). The former case may reflect a transition stage to the latter case.
From the above results, we can infer that the SAM of shl2-8 mutants disappears during development. The shl2-8 SAM is initiated incompletely due to an insufficient number of indeterminate cells. This initial defective state seriously affects subsequent SAM development. The SAM is gradually consumed by leaf primordia and the number of indeterminate cells is progressively reduced. Finally, SAM identity is lost and development terminates after the SAM is converted into a leaf primordium.
To investigate the general function of the SHL2 gene in the establishment and maintenance of the SAM, we regenerated adventitious shoots from scutellum-derived calli. In contrast to the failure of adventitious shoot induction from calli of strong shl2 alleles (
Development of the weak shl1-3 mutant:
The shl1-3 mutant followed a developmental course similar to that of shl2-8. In shl1-3 strains, SAM initiated in 84% of embryos, in contrast to the lack of SAM in 94% of strong shl1-1 embryos. However, the SAM was not observed in 70% of mature embryos, indicating that the SAMs formed in the early embryos disappeared after producing 1–3 leaf primordia (Fig 8A). Thus, SHL1 gene as well as SHL2 gene is required not only for initiation but also for maintenance of the SAM. The expression of OSH1 was examined in the embryos just before SAM initiation. The expression domain of OSH1 in shl1-3 embryo was larger than that in the strong allele shl1-2 embryo (Fig 8B and Fig C), as observed in the weak alleles of shl2. Again, the size of OSH1-expression domain was positively correlated with the frequency of SAM initiation between the weak and strong alleles.
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The development of shl1-3 plants was similar to that of shl2-8. After germination, shl1-3 seedlings rapidly produced thread-like leaves in an irregular phyllotaxy (Fig 8D) and showed frequent expression of histone H4 gene in the SAM (Fig 8E). In the SAM, the OSH1 expression was restricted (Fig 8F). Frequently, a trichome was produced from the tip of the SAM (Fig 8G). Finally, the SAM was converted to leaf primordium, and the plants died <2 months after germination.
shl2 sho2 double mutant:
The phenotypes of seedlings and adventitious shoots of weak shl2 and shl1 mutants were very similar to those of shoot organization (sho) mutants (Fig 9;
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To determine the genetic interaction between SHL2 and SHO, we constructed shl2-3 sho2 and shl2-6 sho2 double mutants. The shl2-3 is a strong allele showing almost no SAM formation in embryo. In F2 progeny, normal, shl2-3, and sho2 embryos segregated in the ratio of 114:50:38, well fitted to the expected 9:4:3 ratio, indicating that SHL2 is epistatic to SHO2. The shl2-6 shows more severe phenotypes than shl2-7 and shl2-8 do, and the sho2 phenotype is weaker than those of the other sho mutants. Therefore, it is relatively easy to discriminate between shl2-6 and sho2 mutants in embryos and seedlings. The F2 progeny of F1 plants heterozygous for both loci segregated, as expected, for shl2-6 and sho2 embryos. The F2 progeny were classified as normal, shl2-6, and sho2 phenotypes. Among the F2 embryos and seedlings, we could not detect a double-mutant phenotype distinct from each single mutant. The segregation value of F2 embryos derived from three F1 plants was normal:shl2-6:sho2 = 47:29:14, not significantly deviating from the expected 9:4:3 ratio. Thus shl2 is epistatic to sho2, suggesting that SHL2 functions upstream of SHO2 in a pathway regulating SAM development.
| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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This study has demonstrated that weak shl2 and shl1 alleles cause defects in both initiation and maintenance of the SAM. In addition, abnormalities were also detected in the initiation pattern of leaf primordia and in leaf morphogenesis. Accordingly, SHL2 and SHL1 genes play a fundamental role during multiple stages of shoot development.
Function of SHL2 and SHL1 genes in shoot development:
In a previous report (
To date very few loci have been reported accounting for both initiation and maintenance of the SAM. In Arabidopsis, the STM gene functions in both initiation and maintenance of the SAM (
In Arabidopsis, WUS and CLV3 genes are required for SAM maintenance through retaining stem cells (
Interestingly, phyllotaxy and plastochron are also affected in shl2-8 and shl1-3 mutants. These phenotypes may result from the aberrant SAM organization. It is known that modified phyllotaxy/plastochron is associated with a change in SAM shape and/or size (
Abnormalities are also detected in shl2 leaves, including abnormal histogenesis at the early seedling stage such as extra cell divisions in the adaxial epidermis and enlarged air space in the proximal region. In sho mutants, which show phenotypes similar to those of shl2-8, no histological abnormalities in leaves are observed, although the leaf shape is severely affected (
Novel aspect of SAM initiation:
Although several mutants defective in SAM initiation have been identified in Arabidopsis (
As seen in Fig 3 and Table 2, it is clear that a positive correlation exists between the size of OSH1-expression domain and the frequency of SAM initiation and the duration of SAM maintenance. In other words, the extent of SAM initiation and maintenance depends on how many (indeterminate) cells are recruited into the SAM. This indicates that SAM formation is not an all-or-nothing process. SAM is constructed in various degrees, depending on how many indeterminate cells are recruited into the SAM. As a result, when the SAM domain (the number of indeterminate cells) is small, the SAM is not produced as in strong shl2 alleles, but when it is intermediate, SAM is incompletely and transiently formed as observed in weak shl2 alleles. From the comparison of many shl2 alleles (Fig 3), we could quantitatively estimate the threshold values for SAM formation: 30 cells for the initiation and 80–90 cells for normal construction. At present, it is still unclear whether the number 30 has some general meaning such that an organ primordium needs at least 30 founder cells for initiation. In addition, the initial number of indeterminate cells for SAM is correlated with the duration of SAM maintenance. Thus, incompleteness at the initial step affects the subsequent activity of SAM. Incompletely initiated SAMs of weak shl2 alleles are not recovered, but are transiently maintained. This aspect of SAM formation has not been reported in other plants.
Functional redundancy between SHL2 and SHO genes:
The embryo and seedling phenotypes of shl2-8 are very similar to those of sho mutants (
In this study, we show that the SHL2 and SHL1 genes are required for both initiation and maintenance of the SAM and are also involved in the initiation and morphogenesis of leaf primordia. Whether the other SHL genes function in shoot development after SAM formation remains to be shown.
| ACKNOWLEDGMENTS |
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We thank David Jackson (Cold Spring Harbor Laboratory) and Hidemi Kitano (Nagoya University) for critical reading of the manuscript. We also thank Makoto Matsuoka (Nagoya University) for providing OSH1 and histone H4 probes. Noboru Washizu, Ken-Ichiro Ichikawa, and Chihiro Sasaki helped us with the cultivation of rice plants in the Experimental Farm of the University of Tokyo. This work was supported in part by a Grant-in-Aid for Scientific Research on Priority Areas (grant 14036206) from the Ministry of Education, Science, and Culture of Japan.
Manuscript received November 14, 2002; Accepted for publication January 21, 2003.
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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