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, 27 (4), 1173-84

Axillary Meristem Formation in Rice Requires the WUSCHEL Ortholog TILLERS ABSENT1

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Axillary Meristem Formation in Rice Requires the WUSCHEL Ortholog TILLERS ABSENT1

Wakana Tanaka et al. Plant Cell.

Abstract

Axillary shoot formation is a key determinant of plant architecture. Formation of the axillary shoot is regulated by initiation of the axillary meristem or outgrowth of the axillary bud. Here, we show that rice (Oryza sativa) TILLERS ABSENT1 (TAB1; also known as Os WUS), an ortholog of Arabidopsis thaliana WUS, is required to initiate axillary meristem development. We found that formation of the axillary meristem in rice proceeds via a transient state, which we term the premeristem, characterized by the expression of OSH1, a marker of indeterminate cells in the shoot apical meristem. In the tab1-1 (wus-1) mutant, however, formation of the axillary meristem is arrested at various stages of the premeristem zone, and OSH1 expression is highly reduced. TAB1/WUS is expressed in the premeristem zone, where it shows a partially overlapping pattern with OSH1. It is likely, therefore, that TAB1 plays an important role in maintaining the premeristem zone and in promoting the formation of the axillary meristem by promoting OSH1 expression. Temporal expression patterns of WUSCHEL-RELATED HOMEOBOX4 (WOX4) indicate that WOX4 is likely to regulate meristem maintenance instead of TAB1 after establishment of the axillary meristem. Lastly, we show that the prophyll, the first leaf in the secondary axis, is formed from the premeristem zone and not from the axillary meristem.

Figures

Figure 1.
Figure 1.
Phenotypes of the tab1-1 Mutant. (A) and (B) Shoot phenotypes of 2-month-old plants. (C) and (D) Phenotypes of panicles. (E) and (F) Complementation of tab1-1. Shown are a plant producing tillers (arrowheads) 2 months after regeneration (E) and a panicle with normal branches and spikelets (F). All six regenerated shoots with the TAB1 genomic sequence showed phenotypes similar to the wild type. (G) and (H) Phenotypes of spikelets. (I) and (J) Expression pattern of OSH1. (K) and (L) Phenotypes of branches. rg, rudimentary glume; sl, sterile lemma; sm, spikelet meristem. Bars in (A) to (F), (K), and (L) = 2 cm; bars in (G) and (H) = 1 mm; bars in (I) and (J) = 50 μm.
Figure 2.
Figure 2.
Comparison of Shoot Phenotypes between the Wild Type and tab1-1. Comparison of the number of tillers, leaves, and spikelets per primary branch between the wild type and tab1-1 (2-month-old plants) is shown. Asterisks indicate significant differences from the wild type (Student’s t test, P < 1 × 10−21 [A], P < 1 × 10−3 [C]). ns, not significant. Error bars indicate se.
Figure 3.
Figure 3.
Effect of tab1-1 Mutation on the Axillary Buds. (A) to (C) Basal region of the culm of 3-week-old plants after the removal of leaves. Arrowheads indicate the axillary buds in the wild type (A) and abnormal buds in tab1-1 ([B] and [C]). Complete absence of an axillary bud (type I) and putative type II axillary buds are indicated by the dashed and solid lines, respectively. (D) to (F) Scanning electron microscopy images of the region where the axillary bud is formed. Arrowheads indicate a normal prophyll in the wild type (D) and a highly reduced prophyll in tab1-1 (E). No prophyll-like structure is observed in (F). (G) and (H) Cross sections of the axillary bud in the wild type (G) and a type II axillary bud in tab1-1 (H). (I) to (L) Longitudinal sections of the axillary bud in the wild type ([I] and [J]) and an abnormal bud in tab1-1 ([K] and [L]). Note that the images in (I), (K), and (L) are shown at the same magnification. (M) and (N) Schematic representations of tiller bud production in each leaf axil of the wild type and tab1-1 in 2-week-old seedlings (M) and 4-week-old seedlings (N). Each column stands for a single plant, and each row stands for a leaf axil in order from bottom to top. Green, normal axillary bud; dark green, elongated axillary bud after release from dormancy; yellow, absence of axillary bud (type I); gray, putative type II axillary bud; brown, type III axillary bud showing an abnormally elongated prophyll. am, axillary meristem; lvb, large vascular bundle. Bars in (A) to (C) = 1 mm; bars in (G) to (L) = 200 μm; bars in (D) to (F) = 500 μm.
Figure 4.
Figure 4.
Developmental Patterns of Axillary Buds in the Wild Type and tab1-1. (A) to (E) Longitudinal sections of the shoot apex (A) and the region where the axillary buds initiate ([B] to [E]). (F) to (J) Expression patterns of OSH1 during the formation of axillary buds in the wild type. Brackets indicate the premeristem zone. (K) to (M) Longitudinal sections of the region where the axillary buds should form in tab1-1. Development of the premeristem zone was terminated in some plants ([K] and [L]), and an abnormally elongated prophyll was formed in others (M). The arrowhead indicates flattened tissue where the meristem dome would form in the wild type. (N) to (P) Expression patterns of OSH1 in tab1-1. Arrowheads and the asterisk indicate very weak ([N] and [P]) and narrow (O) expression of OSH1. am, axillary meristem; ap, abnormal prophyll; pp, prophyll. Bars = 50 μm.
Figure 5.
Figure 5.
Expression Patterns of MOC1 and LAX1 during Axillary Bud Formation. (A) and (B) Expression patterns of MOC1. (C) to (F) Expression patterns of LAX1. Bars = 50 μm.
Figure 6.
Figure 6.
Spatial Expression Patterns of TAB1 and WOX4 in the Wild Type. (A) to (D) Expression of TAB1 in the premeristem zone and the axillary bud. No TAB1 expression is observed in developing (C) and established (D) axillary buds. (E) to (G) Expression patterns of TAB1 (E), OSH1 (F), and WOX4 (G) in the SAM of a 4-week-old wild-type seedling. (H) to (K) Expression of WOX4 in the premeristem zone ([H] and [I]) and the axillary bud ([J] and [K]). No WOX4 expression is observed in the premeristem zone ([H] and [I]). Brackets indicate the premeristem zone. am, axillary meristem; pp, prophyll. Bars = 50 μm.
Figure 7.
Figure 7.
Schematic Representation of Axillary Bud Development in Rice. Brackets indicate the premeristem zone. The expression domains of TAB1 and OSH1 are indicated with yellow and pink, respectively. am, axillary meristem.

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