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Grassy tillers1 Promotes Apical Dominance in Maize and Responds to Shade Signals in the Grasses

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Grassy tillers1 Promotes Apical Dominance in Maize and Responds to Shade Signals in the Grasses

Clinton J Whipple et al. Proc Natl Acad Sci U S A.

Abstract

The shape of a plant is largely determined by regulation of lateral branching. Branching architecture can vary widely in response to both genotype and environment, suggesting regulation by a complex interaction of autonomous genetic factors and external signals. Tillers, branches initiated at the base of grass plants, are suppressed in response to shade conditions. This suppression of tiller and lateral branch growth is an important trait selected by early agriculturalists during maize domestication and crop improvement. To understand how plants integrate external environmental cues with endogenous signals to control their architecture, we have begun a functional characterization of the maize mutant grassy tillers1 (gt1). We isolated the gt1 gene using positional cloning and found that it encodes a class I homeodomain leucine zipper gene that promotes lateral bud dormancy and suppresses elongation of lateral ear branches. The gt1 expression is induced by shading and is dependent on the activity of teosinte branched1 (tb1), a major domestication locus controlling tillering and lateral branching. Interestingly, like tb1, gt1 maps to a quantitative trait locus that regulates tillering and lateral branching in maize and shows evidence of selection during maize domestication. Branching and shade avoidance are both of critical agronomic importance, but little is known about how these processes are integrated. Our results indicate that gt1 mediates the reduced branching associated with the shade avoidance response in the grasses. Furthermore, selection at the gt1 locus suggests that it was involved in improving plant architecture during the domestication of maize.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Phenotypic characterization of gt1. (A) gt1-1 tassel floret, with anthers removed to reveal the growth of a deformed carpel-like organ surrounded by three stamen filaments and two lodicules. ca, carpel-like organ; lo, lodicule; st fil, stamen filament. (B) WT tassel floret with anthers removed shows no carpel growth; only stamens filaments and lodicules are present. (C) gt1-1 mutant in B73 background with tillers (arrows). (D) WT B73 with no tillers. (E) Ear from a gt1-1 mutant, with the arrow indicating a prominent blade on a husk leaf. (F) Ear from WT B73 has no blades on husk leaves. (G) Graph showing a comparison of ear number, tiller number, and ear shank length between gt1-1 and the isogenic WT A619. The gt1-1 mutants have significantly more tillers and ears, with longer ear branches. Error bars indicate the 95% confidence interval. The scale to the left (number) is for ear and tiller number, whereas the scale to the right (cm) is for ear shank length. (H) Graph as in G showing a comparison of an F1 between A619 and gt1-1 (gt1-1/+) with WT A619 (+/+). Although the heterozygote has no tillers, it does have a significant increase in ear number and ear shoot length, indicating that gt1-1 is not fully recessive.
Fig. 2.
Fig. 2.
Cloning and expression of gt1. (A) Genomic region on maize chromosome 1S containing gt1-1 as determined by positional cloning. Most closely linked markers are indicated by arrowheads, with the recombination frequency and direction of recombinants underneath. (B) Phylogenetic analysis of gt1 and closely related genes from grasses (sorghum, Brachypodium, rice, and maize) and Arabidopsis. The paralogous gt1 and Vrs1 grass clades are indicated. Nodal support is indicated as Bayesian posterior probability. (C) Gene model for gt1, with position of lesions in mutant alleles gt1-1, gt1-mum1, and gt1-ref indicated. A CAPS marker for the G > A splice site mutation in gt1-1 was completely linked in our mapping population of 352 chromosomes, whereas a nearby intragenic MspI polymorphism showed recombination, indicating that the gt1 locus is in a region of high recombination. (D) In situ RNA hybridization of gt1 on a maize shoot apex. Short exposure revealed strong expression in leaves and provasculature of lateral buds (arrows and Inset) but no expression in the shoot apical meristem (*) or surrounding leaves. (E) Higher magnification of boxed lateral bud in D showing gt1 expression in the adaxial domain of surrounding leaf primordia but absent from the meristem (*). (F) Longer exposure revealed gt1 expression in the leaf primordia surrounding the shoot apex, apparently attributable to a lower level of expression than that present in the lateral buds (* indicates apical meristem). (G) gt1 is strongly expressed in degenerating carpel primordium of young tassel florets and weakly expressed in the palea and outer glume but is absent from stamen primordia. ca, carpel primordium; pal, palea; og, outer glume; st, stamen primordia. (Inset) Transverse section of a tassel floret with gt1 expression in a ring at the base of the carpel. (H) GT1-YFP expression in both the leaf primordia and the axillary meristem of a lateral tiller bud. AxM, axillary meristem; LP, leaf primordia. (I) GT1-YFP nuclear localization in the leaf primordium of lateral bud. (Inset) Magnified view.
Fig. 3.
Fig. 3.
Regulation of gt1 by light in teosinte and sorghum. Plant height (A) and length (B) of buds in the first leaf axil of teosinte seedlings at 11 d after planting grown without supplemental FR light (Control) and with supplemental FR light for 2 d starting at 9 days after planting. Error bars represent SE of seedling height and bud length of 9 or 10 seedlings. (C) Relative expression level of gt1 in axillary buds of FR-treated or control teosinte seedlings determined by quantitative real-time PCR. Error bars represent SE of three biological replicates, each from at least 3 axillary buds. (D) Relative expression level of the sorghum Gt1 (SbGt1) in WT and phyB-1 mutant axillary buds in the first leaf axil. DAP, days after planting. The expression level of SbGt1 was measured using quantitative RT-PCR. Error bars represent SE of two biological replicates, each from at least 10 axillary buds.
Fig. 4.
Fig. 4.
Interactions between gt1 and tb1. (A) Bud length and relative tb1 expression level were measured in WT (A619) and homozygous gt1-1 mutant seedlings. (B) Bud length and relative gt1 expression level were measured in heterozygous tb1-ref/+ and homozygous tb1-ref mutants. Error bars represent SE of 30 axillary buds for WT and gt1-1 mutant seedlings and three biological replicates for the expression of tb1, each from at least four axillary buds. For the tb1 mutants, error bars represent SE of the length and expression of gt1 in eight and seven axillary buds of heterozygous tb1-ref/+ and homozygous tb1-ref mutants, respectively. No detectable gt1 expression above background is indicated by an asterisk for tb1-ref/tb1-ref. (C) Model for light regulation of axillary bud growth in grasses. Perception of shading (low R/FR) via the phytochromeB photoreceptor (phyB) initiates a signaling cascade in the leaves, which ultimately transports a signal to the axillary bud that promotes tb1 transcription. tb1 expression promotes gt1 expression, leading to suppression of lateral bud outgrowth in the shade.
Fig. P1.
Fig. P1.
(A) WT maize with no tillers. (B) gt1 mutant with increased tiller growth (arrows). (C) In situ RNA hybridization of gt1 on a section through the maize shoot apex. Strong expression is observed in the leaves and provasculature of lateral buds (arrows and Inset) but not in the shoot apical meristem (*) or surrounding leaves. (D) Higher magnification of the lateral bud (Inset in C) shows Gt1 expression in the adaxial domain of surrounding leaf primordia but absent from the meristem (*). (E) GT1-YFP expression in both the leaf primordia and the axillary meristem of a lateral tiller bud. AxM, axillary meristem; LP, leaf primordia. (F) Model for light regulation of axillary bud growth in maize. Perception of shading (low R/FR) via the phyB photoreceptor initiates a signaling cascade in the leaves, which ultimately transports a signal to the axillary bud that promotes tb1 transcription. tb1 expression promotes gt1 expression, leading to repression of lateral bud outgrowth in the shade. R:FR, R/FR.

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