Os10g0478000
The rice TAWAWA1 (TAW1) gene, a member of ALOG family, was identified as a regulator of rice inflorescence architecture.
Contents
Annotated Information
Function
In the dominant gain-of-function mutant tawawa1-D (Fig. 1), 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 branch meristem (BMs). TAW1 expression disappears from incipient spikelet meristems (SMs). It is demonstrated that members of the SHORT VEGETATIVE PHASE subfamily of MADS-box genes function downstream of TAW1. Thus, TAW1 is proposed as 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 [1].
To understand the molecular links between the control of meristem phase transition and inflorescence structure, mutants were identified with altered inflorescence branching patterns [1]. Two lines with increased branching phenotypes were isolated from a screening population in which nDart1, an endogenous rice transposon, actively transposes (Fig. 1C). The mutation was inherited in a semidominant manner in both lines, and subsequent analyses revealed mutations in the same gene. The gene was named TAWAWA1 (TAW1), from a traditional Japanese word meaning “very fruitful.” taw1-D1 exhibits more severe defects than those of taw1-D2. Both mutant lines show normal growth patterns during the vegetative phase, for example, meristem size, date of leaf initiation, and number of leaves produced. However, in taw1-D1 homozygous plants, stem elongation is suppressed after the transition to reproductive growth, and the inflorescence does not emerge from the leaves. In both mutant lines, the number of lateral meristems produced on each primary branch is comparable to that of wild-type plants; however, a higher percentage of lateral meristems grows as secondary branches (Fig. 1D). Reiteration of this pattern results in the production of tertiary branches, which are not formed on wild-type plants (Fig. 1E).
In homozygous taw1-D1 mutants (carrying the more severe allele), the increase in inflorescence branching is so extreme that the inflorescence forms an agglomerate with a massive number of undifferentiated meristems (Fig. 1 F and G). Such aggregated meristems are also frequently observed in the inflorescences of taw1-D1 heterozygous and taw1-D2 homozygous plants (Fig. 1 H and I). Observations using a scanning electron microscope confirmed that these structures are formed from the repeated production of undifferentiated meristems (Fig. S2). The meristems in taw1-D1 homozygous inflorescences were analyzed for expression of two SM marker genes, FRIZZY PANICLE (FZP) and LEAFY HULL STERILE1 (LHS1)/OsMADS1, by in situ hybridization. The lack of expression of these genes indicated that the meristems in the homozygous mutants do not acquire SM identity (Fig. 1 J–M).
Grain number per panicle is one of the four major determinants of rice yield. To test the usefulness of TAW1 mutations for increasing grain yield, the moderate taw1-D2 allele was introgressed into Koshihikari, which is a leading commercial rice cultivar in Japan (Fig. 5 A and B). Field-grown selfed progeny of fifth backcross (BC5F2)-generation plants showed ∼45% increases in grain weight per plant (Fig. 5C). These increases were mainly due to extensive increases in grain number per panicle (Fig. 5D), resulting from increases in the numbers of primary, secondary, and tertiary branches. Slight decreases in fertility and grain weight were also observed (Fig. 5E). Despite the increase in panicle size, the total plant height was slightly reduced in BC5F2 plants. Increases in grain number are often linked to decreases in the numbers of branch shoots, called “tillers,” in rice. However, this tradeoff effect was not observed in the taw1-D2 introgression line.
Expression
TAW1 contains a conserved domain and a nuclear localization signal. Indeed, TAW1 localizes to the nucleus and shows slight but significant activity as a transcriptional activator (Fig. 3 A and B). The spatiotemporal pattern of TAW1 mRNA accumulation was examined by in situ hybridization. During the vegetative phase of development, TAW1 was predominantly expressed in meristems, including the SAM, axillary meristems, and young leaves (Fig. 3 A and C). After transition to the reproductive phase, TAW1 mRNA continued to accumulate in the IM (Fig. 3D). The strongest signal was observed in BMs in the growing inflorescence (Fig. 3E). After initiation of the primary BMs, TAW1 expression gradually disappeared from the IM as it degenerated (Fig. 3F). In wild-type inflorescences, the signal intensity in the meristem gradually decreased and became undetectable at SM initiation (Fig. 3G). On the other hand, in taw1-D inflorescences, stronger TAW1 signals were detected, even at the stage when the SMs were formed in the wild-type plants (Fig. 3 H and I). Quantitative PCR analysis indicated that the levels of TAW1 expression in the mutant inflorescences roughly coincided with the severity of their phenotypes (Fig. 3J). These results imply that TAW1 functions to suppress SM identity and that its activity must be below a certain threshold level to allow SM specification. Interestingly, TAW1 expression is reduced in the vegetative shoot apices, leaves, and roots of taw1-D mutants compared with wild-type plants. These results suggest that the sequence surrounding the nDart1 insertion sites is necessary for fine-tuning the spatial and quantitative expression pattern of TAW1. It may be that positive regulators of SM identity interact with this sequence, which is located downstream of the transcribed region. It is also possible that nDart1 carries a sequence that functions as a transcriptional enhancer; however, this is unlikely because not all nDart1 insertions activate transcription. Unraveling the molecular mechanisms that regulate TAW1 transcription will shed light on the regulatory networks controlling rice inflorescence architecture.
The rice genes G1 and TH1 are ALOG family members that are expressed in the lemma, palea, and floral organs and control their identity and development. On the other hand, the Arabidopsis ALOG family genes LSH3/OBO1 and LSH4 are expressed in shoot organ boundary cells. The functions of LSH3/OBO1 and LSH4 are unknown; however, they induce the overproliferation of shoot meristems and the formation of extra organs when ectopically expressed. A plausible scenario is that at least some of the ALOG family proteins share conserved functions, but it may be that their distinctive expression patterns have led to divergent functions. The establishment of the machinery for meristem-specific expression may be a primary reason for the evolution of TAW1 as a major regulator of meristem activity and phase transition [1].
Evolution
TAW1 function might have evolved to ensure the production of sufficient numbers of spikelets. Unraveling the molecular function of TAW1 will provide an opportunity for a greater understanding of meristem activity and identity, which is a fundamental issue in plant biology. Furthermore, such knowledge could be exploited to further increase crop yields. In addition, TAW1 is of great interest with respect to the evolution of inflorescence architecture. TAW1 function may be essential for the development of compound inflorescences, in which the branching pattern is crucial [1].
Labs working on this gene
- Graduate School of Agriculture and Life Sciences, The University of Tokyo, Yayoi, Bunkyo, Tokyo 113-8657, Japan
