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, 110 (2), 767-72

TAWAWA1, a Regulator of Rice Inflorescence Architecture, Functions Through the Suppression of Meristem Phase Transition

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TAWAWA1, a Regulator of Rice Inflorescence Architecture, Functions Through the Suppression of Meristem Phase Transition

Akiko Yoshida et al. Proc Natl Acad Sci U S A.

Abstract

Inflorescence structures result from the activities of meristems, which coordinate both the renewal of stem cells in the center and organ formation at the periphery. The fate of a meristem is specified at its initiation and changes as the plant develops. During rice inflorescence development, newly formed meristems acquire a branch meristem (BM) identity, and can generate further meristems or terminate as spikelets. Thus, the form of rice inflorescence is determined by a reiterative pattern of decisions made at the meristems. In the dominant gain-of-function mutant tawawa1-D, the activity of the inflorescence meristem (IM) is extended and spikelet specification is delayed, resulting in prolonged branch formation and increased numbers of spikelets. In contrast, reductions in TAWAWA1 (TAW1) activity cause precocious IM abortion and spikelet formation, resulting in the generation of small inflorescences. TAW1 encodes a nuclear protein of unknown function and shows high levels of expression in the shoot apical meristem, the IM, and the BMs. TAW1 expression disappears from incipient spikelet meristems (SMs). We also demonstrate that members of the SHORT VEGETATIVE PHASE subfamily of MADS-box genes function downstream of TAW1. We thus propose that TAW1 is a unique regulator of meristem activity in rice and regulates inflorescence development through the promotion of IM activity and suppression of the phase change to SM identity.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Characterization of taw1 dominant mutants. (A) Schematic of a rice inflorescence, called a “panicle.” DTP, degenerate tip of the rachis; LS, lateral spikelet; PB, primary branch; SB, secondary branch; TS, terminal spikelet. (B) A conceptualized view of meristem identity specification. A newly formed meristem (green) acquires either a spikelet meristem (pink) identity or a branch meristem (blue) identity. The SM produces a flower and terminates. The BM continues to produce next-order meristems that repeat the same step. The BM eventually acquires an SM identity and grows as a terminal spikelet. Black arrows indicate initiation of an additional meristem. (C) Inflorescence of taw1-D mutants. (D) Number of lateral meristems generated on a primary branch. The blue bottom bar indicates secondary branches and the pink upper bar indicates lateral spikelets. Asterisks indicate a significant difference from corresponding control (WT) samples (Student’s t test; **P < 0.01). (E) Frequency of tertiary branch formation. In D and E, n = 27, 28, and 25 for WT, taw1-D2/+, and taw1-D2, respectively. (F) Immature inflorescence of the taw1-D1 homozygous plant. (G) Close-up of the taw1-D1 inflorescence shown in F. (H and I) taw1-D2 homozygous inflorescence. An aggregation of branch meristems boxed in H is shown in I. (JM) Expression of spikelet meristem marker genes FRIZZY PANICLE (J and K) and LEAFY HULL STERILE1 (L and M) in wild-type (J and L) and taw1-D1 homozygous plant (K and M) inflorescences at the spikelet meristem initiation stage. (Insets) A spikelet meristem is shown.
Fig. 2.
Fig. 2.
Isolation of the TAW1 gene. (A) Insertion of nDart1-0 into a region on chromosome 4 cosegregated with the inflorescence phenotype. (B) Expression levels of genes surrounding the insertion sites in immature inflorescences. Values represent the expression level in heterozygous (taw1-D1/+) and homozygous (taw1-D1) mutants relative to that of wild-type plants. (C) Inflorescences in taw1-3 and its WT plants T65 (Taichung 65). (D) Number of primary branches per inflorescence. n = 7, 5, 9, and 7 for WT (T65), taw1-3, WT (N), and taw1-4, respectively. Asterisks indicate a significant difference from corresponding control samples (Student’s t test; **P < 0.01). (E) Inflorescences in RNAi and WT plants.
Fig. 3.
Fig. 3.
Expression pattern of TAW1. (A and B) Localization of TAW1-GFP fluorescence in the rice shoot at the vegetative stage. The TAW1-GFP construct was expressed under the control of regulatory sequences from the TAW1 gene. The construct was introduced into taw1-3 and the rescue of the mutant phenotype was confirmed. A part of the young leaf boxed in A is shown in B. (CG) In situ hybridization analysis of TAW1 expression in the vegetative shoot apex (C), inflorescence meristem (D), very young inflorescence at the early primary branch initiation stage (E), very young inflorescence at the late primary branch initiation stage (F), and an immature inflorescence at the spikelet meristem initiation stage (G) in wild-type plants. White arrowheads, leaf primordia; red arrowheads, primary branch meristem. (H and I) TAW1 expression in the taw1-D1 homozygous inflorescence at the SM meristem initiation stage. The TAW1 signal was more intense in taw1-D1 than in wild-type and the signal continued in the immature panicle at the stage when SMs initiate (H) and even at later stages (I). (J) Quantitative RT-PCR analysis of TAW1 expression in the inflorescence at the spikelet initiation stage. The values represent mean TAW1 expression relative to UBIQUITIN ± SD (n = 3).
Fig. 4.
Fig. 4.
SVP subfamily MADS-box genes work downstream of TAW1. (A) Expression levels of 32 MADS-box genes in young inflorescences of taw1-D2/+ (blank) and taw1-D2 (colored) plants, relative to that of wild-type plants. (B and C) Expression of OsMADS47 in the immature inflorescence at the secondary branch initiation stage in wild-type (B) and taw1-D1 (C). (D) Induction of OsMADS22 and OsMAD55 transcription by TAW1. Relative values of TAW1, OsMADS22, and OsMADS55 expression in wild-type and pINDEX-TAW1 plants in the presence (+) or absence (−) of dexamethasone treatment are shown. Values are means ± SD (n = 3). (E) Inflorescence morphologies in 35S:OsMADS22 (OsMADS22ox) and 35S:OsMADS55 (OsMADS55ox) plants. Yellow asterisks indicate secondary branches.
Fig. 5.
Fig. 5.
Phenotype of taw1-D2–introgressed Koshihikari BC5F2 plants. (A and B) The plant (A) and panicle (B) of Koshihikari (K) (Left) and taw1-D2 BC5F2 plants (Right). Tertiary branches are marked with yellow asterisks. (C) Total grain weight per plant in grams. (D) Number of grains per panicle. (E) One thousand grain weight in grams. In CE, n = 23 plants for Koshihikari and 24 plants for BC5F2 homozygous taw1-D2. All data are shown as means ± SD. Asterisks indicate a significant difference from corresponding control samples of Koshihikari (Student’s t test; *P < 0.05, **P < 0.01).

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