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First published online January 27, 2006; 10.1104/pp.105.074856 Plant Physiology 140:1109-1117 (2006) © 2006 American Society of Plant Biologists Phytochrome B Represses Teosinte Branched1 Expression and Induces Sorghum Axillary Bud Outgrowth in Response to Light Signals1Department of Soil and Crop Sciences (T.H.K., S.A.F.), and United States Department of Agriculture Agricultural Research Service (B.L.B.), Texas A&M University, College Station, Texas 77843–2474
Light is one of the environmental signals that regulate the development of shoot architecture. Molecular mechanisms regulating shoot branching by light signals have not been investigated in detail. Analyses of light signaling mutants defective in branching provide insight into the molecular events associated with the phenomenon. It is well documented that phytochrome B (phyB) mutant plants display constitutive shade avoidance responses, including increased plant height and enhanced apical dominance. We investigated the phyB-1 mutant sorghum (Sorghum bicolor) and analyzed the expression of the sorghum Teosinte Branched1 gene (SbTB1), which encodes a putative transcription factor that suppresses bud outgrowth, and the sorghum dormancy-associated gene (SbDRM1), a marker of bud dormancy. Buds are formed in the leaf axils of phyB-1; however, they enter into dormancy soon after their formation. The dormant state of phyB-1 buds is confirmed by the high level of expression of the SbDRM1 gene. The level of SbTB1 mRNA is higher in the buds of phyB-1 compared to wild type, suggesting that phyB mediates the growth of axillary shoots in response to light signals in part by regulating the mRNA abundance of SbTB1. These results are confirmed by growing wild-type seedlings with supplemental far-red light that induces shade avoidance responses. We hypothesize that active phyB (Pfr) suppresses the expression of the SbTB1 gene, thereby inducing bud outgrowth, whereas environmental conditions that inactivate phyB allow increased expression of SbTB1, thereby suppressing bud outgrowth.
The highly ordered arrangement of leaves and branches and the final shoot architecture are associated with a plant's developmental strategy to ensure its survival and productivity under continuously changing growing conditions. A complex developmental program that integrates genetic mechanisms, physiological processes, and environmental signals controls the overall form of the plant. The shoot architecture of crop plants has been modified during their domestication and improvement. One of the great achievements in the history of crop improvement, "The Green Revolution," was due to dwarfing of wheat (Triticum aestivum) and other crops to increase nitrogen-use efficiency and reduce lodging. A more complete understanding of the developmental programs that control shoot architecture will help to further improve resource-use efficiency and yield of crop plants.
Shoot architecture is largely determined by the number of axillary shoots produced. Axillary shoot development begins with the initiation of an axillary meristem in the axil of a leaf to form a bud (for review, see Ward and Leyser, 2004
Molecular and genetic approaches have been used to study the mechanisms of action of plant hormones and to identify genes involved in regulating branching. Genes that control axillary meristem initiation have been identified in various species (Schumacher et al., 1999
A genetic analysis of the morphological differences between maize (Zea mays subsp. mays) and its wild ancestor teosinte (Zea mays subsp. parviglumis) led to the cloning of the Teosinte Branched1 (TB1) gene (Doebley et al., 1997
Several genes that are specifically up-regulated or down-regulated during branching have been identified. The dormancy-associated genes of pea, PsDRM1 (Stafstrom et al., 1998b
It is well established that light quality (red:far red [R:FR]) is one of the environmental signals that regulate shoot branching (Casal et al., 1986
Plants use light signals perceived by photoreceptors to coordinate all stages of growth and development from germination to flowering. The phytochrome family of photoreceptors is involved in deetiolation, vegetative development, and flowering time in both dicots and monocots (Mathews and Sharrock, 1996 We used the phyB null mutant sorghum (phyB-1) as a model for studying the regulation of branching by light. The strong apical dominance of phyB-1, and the early formation and ease of excising axillary buds make sorghum useful for studying the role of light in axillary shoot development. We asked whether light signals perceived by phyB control shoot branching by regulating the expression of branching genes previously identified in other species. We characterized the enhanced apical dominance in phyB-1 sorghum and investigated the expression of branching-related genes, including the sorghum homologs of the TB1 (SbTB1) and dormancy-associated (SbDRM1) genes in phyB-1 and wild-type axillary buds. In this article, we report the regulation of expression of the sorghum SbTB1 and SbDRM1 genes by light signals perceived by phyB, and phyB's association with dormancy and outgrowth of axillary buds.
Enhanced Apical Dominance in phyB-1 Mutant Sorghum The phyB-1 mutant sorghum fails to produce branches during vegetative development, whereas the near-isogenic wild-type plants branch profusely. The branching deficiency in phyB-1 could theoretically arise from either a defect in axillary meristem initiation or bud outgrowth. We found that the defect occurs in bud outgrowth since equivalent buds are formed early in the development in both phyB-1 and wild-type sorghum (Fig. 1 ). The buds in the axil of the first leaf of both phyB-1 and the wild type grow at the same rate until 7 d after planting (DAP). Then they begin to show different developmental fates (Fig. 2A ). While the buds of the wild type continue elongation, bud outgrowth is inhibited in phyB-1. Axillary buds are formed at all nodes of the main shoot of phyB-1 (data not shown). These buds remain dormant and branching is observed only when the main shoot begins flowering. The phyB-1 seedlings were taller than the wild type, showing enhanced growth of the main shoot as a result of constitutive shade avoidance (Fig. 2B).
Expression of SbTB1 in Different Organs of Sorghum Seedlings
SbTB1 (accession no. AF322132) exists as a single copy in the sorghum genome with 93.9% nucleotide identity with the maize TB1 gene (Lukens and Doebley, 2001
Expression of SbDRM1 in Different Organs of Sorghum Seedlings
PsDRM1 is expressed in dormant axillary buds, and its expression is suppressed by decapitation and auxin (Stafstrom et al., 1998b
Abundance of SbTB1 and SbDRM1 mRNA in phyB-1 and Wild-Type Axillary Buds The expression of the SbTB1 and SbDRM1 genes in sorghum axillary buds was correlated with the dormant state of the buds. At 7 DAP and 9 DAP, SbTB1 mRNA was detected in the axillary buds of both phyB-1 and wild-type seedlings (Fig. 6A ). However, SbTB1 abundance was more than 2-fold higher in the phyB-1 buds compared to the level in the wild type (Fig. 6B). The expression pattern of SbDRM1 was different from that of SbTB1 mRNA. At 7 DAP, when their size was comparable (Fig. 2), SbDRM1 message is hardly detected in the buds of phyB-1 and the wild type (Fig. 6A). At 9 DAP, when the buds of the wild type were rapidly elongating while those of phyB-1 were suppressed, the mRNA level of SbDRM1 was more than 5-fold higher in the buds of phyB-1 than in the wild type (Fig. 6C).
SbTB1 and SbDRM1 mRNA Abundance in Axillary Buds of Wild-Type Seedlings Grown at High and Low Densities The enhanced apical dominance of phyB-1 sorghum is consistent with a constitutive shade avoidance response. Shade avoidance responses are also observed in the natural environment when wild-type plants are grown at high density that lowers the R:FR. In an attempt to simulate the constitutive shade avoidance response of phyB-1 sorghum in the wild type, wild-type seedlings were grown at high (3,000 seedlings m–2) and low (300 seedling m–2) plant densities. In those seedlings grown at a high density, axillary bud outgrowth was suppressed at about 9 DAP (Fig. 7A ). While high density affected axillary bud elongation, the height of seedlings at both planting densities was the same during the measurement period (Fig. 7B).
SbTB1 mRNA accumulation in the buds of wild-type seedlings grown at both plant densities decreased over time (Fig. 8 ). The abundance of SbTB1 mRNA was higher in the axillary buds from high plant density compared to low plant density at both 7 DAP and 9 DAP (Fig. 8). At 7 DAP, SbDRM1 mRNA abundance was only 2.2-fold higher in high density compared to low density (Fig. 9 ). However, relative to wild type at 7 DAP, the level of SbDRM1 mRNA at 9 DAP was increased to 18.6- and 3.7-fold at high and low plant densities, respectively. At 9 DAP, SbDRM1 abundance was therefore 5-fold higher in buds from high compared to low planting density.
SbTB1 and SbDRM1 mRNA Abundance in Axillary Buds of Wild Type Grown with and without Supplemental FR Low R:FR reduces the proportion of the active form of phyB (Pfr), thereby triggering the shade avoidance response. Wild-type seedlings were grown until 7 DAP, when bud length in the axil of the first leaf and seedling height were measured (control, 7 DAP). Then, starting at 7 DAP and continuing for the next 2 d, some of the seedlings were irradiated with FR light from the sides (FR, 9 DAP), while others continued growth without supplemental FR light (control, 9 DAP). The supplemental FR light treatment suppressed the outgrowth of buds in the axil of the first leaf (Fig. 10A ) and increased seedling height (Fig. 10B).
The abundance of SbTB1 and SbDRM1 mRNAs reflects the enhanced apical dominance induced by low R:FR (Fig. 11A ). Compared to the abundance in the control at 7 DAP, the SbTB1 mRNA abundance at 9 DAP was slightly reduced in the control, whereas it was increased in the FR-treated seedlings. The mRNA abundance of SbTB1 was 2.8-fold higher in the FR-treated seedlings compared to the control at 9 DAP (Fig. 11B). The SbDRM1 mRNA level was almost 18-fold higher in axillary buds of seedlings treated with FR compared to control (Fig. 11B).
We investigated the regulation of branching by light signals perceived by phyB in the branching-deficient phyB-1 null mutant sorghum. Mutants used previously to study the molecular mechanisms of branching are defective either in initiation of axillary meristems or outgrowth of buds (Napoli et al., 1999  ; Ward and Leyser, 2004). Our results show that the initiation of axillary meristems and formation of buds occur normally in phyB-1; however, the outgrowth of those buds was inhibited, indicating that the role of light signals in branching is limited to bud dormancy and outgrowth. Bud outgrowth was also inhibited in wild-type plants grown at high plant density or with supplemental FR light, demonstrating the regulation of axillary buds by environmental signals soon after their formation.
Supplemental FR light treatment of wild-type seedlings, started at 7 DAP, inhibited the outgrowth of buds in the first leaf axil of all treated seedlings. However, when FR treatment was started at 9 DAP, the buds in the first leaf axil of some seedlings were arrested, while in others they escaped the inhibitory signal and elongated (data not shown). It is noteworthy that all the buds in the axil of the second leaves of those plants treated with FR at 9 DAP were arrested (data not shown). The inconsistency in the response of buds in the axil of the first leaf to delayed FR light treatment was observed in repeated experiments. The "escape" phenomenon may be similar to the regulation of bud dormancy and outgrowth by auxin (for review, see Cline, 1997 Previous research has indicated that DRM1 expression correlates with bud dormancy, and we have used it here as an indicator of a bud's physiological status. The inhibition of bud outgrowth in phyB-1 sorghum is reflected in the high level of SbDRM1 mRNA in these axillary buds (Fig. 6). The results are confirmed by the high level of SbDRM1 mRNA in the arrested buds of wild type grown at high plant density or with supplemental FR (Figs. 9 and 11). There was a small increase in SbDRM1 mRNA at 9 DAP compared to 7 DAP in wild type grown under standard conditions (Fig. 6) and in wild type grown at low densities (Fig. 9). These results may seem contradictory to the typical correlation of DRM1 expression with dormancy but may indicate an increase in the proportion of nondividing cells in the rapidly elongating buds of the wild type.
The pattern of SbDRM1 accumulation agrees with that observed in pea and Arabidopsis, implying that conserved mechanisms of dormancy and outgrowth may operate in both monocots and dicots—an observation also supported by the orthologous function of MAX-related genes in rice (Ishikawa et al., 2005
The TB1 gene was identified as one of five quantitative trait loci that distinguish the morphology of maize from its wild ancestor, teosinte (Doebley and Stec, 1991
Branching in maize is relatively insensitive to planting density; whereas branching in teosinte is reduced at high plant density and increases at low plant density. Doebley et al. (1995)
It should be noted that the response of wild-type sorghum seedlings to high planting density was not the same as their response to low FR light treatment during the experimental period. Although bud elongation was inhibited in both treatments, only FR induced an increase in seedling height, which is one of the typical shade avoidance responses. The pattern of accumulation of SbDRM1 mRNA at 9 DAP at high planting density and in the FR-treated seedlings was similar in each case, indicating both treatments inhibited bud outgrowth through similar downstream mechanisms. However, the level of SbTB1 mRNA at 9 DAP at high planting density was lower than at 7 DAP at both high and low planting densities (Fig. 8), while FR light treatment increased the level of SbTB1 mRNA at 9 DAP compared to the level at 7 DAP (Fig. 11). Takeda et al. (2003)
SbTB1 mRNA is highest in the younger wild-type buds (7 DAP) and decreases with time, suggesting that early in development these buds acquire a signal that inhibits their outgrowth. The fate of these buds, whether to continue growth or enter into dormancy, is determined at a later stage depending on the perception of light and possibly other signals required for their elongation. The results imply that the absence of active phyB to suppress SbTB1 accumulation in the phyB-1 axillary buds leads to dormancy, while the suppression of SbTB1 accumulation in the wild-type axillary buds by active phyB leads to bud outgrowth. Transgenic potato (Solanum tuberosum) plants overexpressing phyB produced more branches at high plant density (Boccalandro et al., 2003
Devlin et al. (2003)
The TB1 gene belongs to the TCP family of transcription factors with a noncanonical basic helix-loop-helix domain that is predicted to function in DNA-binding and protein-protein interactions (Cubas et al., 1999
It is not yet understood whether hormonal signals interact with TB1 to suppress bud outgrowth (McSteen and Leyser, 2005
Tatematsu et al. (2005)
Plant Materials and Growing Conditions
Wild-type and phyB-1 mutant sorghum (Sorghum bicolor) seedlings were grown in a growth chamber with incandescent and fluorescent lamps, maintained at 31°C/22°C day/night temperatures with a 12-h photoperiod. The photosynthetically active radiation was approximately 600 µmol m–2 s–1 and the R:FR 3.0. Seeds were sown at a rate of 300 m–2 on trays containing 7-cm-deep cells filled with growth medium prepared as described by Beall et al. (1991)
Young elongating shoots of phyB-1 and the wild type were collected about 5 mm from the base of seedlings and fixed in FAA (70% ethanol, 37% formaldehyde-acetic acid, 18:1:1) for at least 24 h, and then stored in 70% ethanol. The young stems were dehydrated in a tertiary butyl alcohol series, embedded in Tissueprep (Fisher Scientific), sectioned at 15 µm with a rotary microtome, and placed on microscope slides that were kept at 40°C to 50°C for at least 24 h. The slides were then stained in Safranin-O fast-green series using an HMS series programmable slide stainer (Carl Zeiss). Two drops of Permount mounting medium (Fisher Scientific) were placed on each slide and covered with a cover glass. The slides were then observed with a bright-field Zeiss microscope.
Subtending leaves were removed, and buds in the axil of the first leaf were excised and their lengths measured under a dissecting microscope using a micrometer. A ruler was used to measure buds longer than 3 mm. Seedling height was also measured as the height from the base of the shoot to the tip of the tallest leaf.
For gene expression studies, seedlings were harvested, roots were washed, and buds in the axil of the first leaves were excised under a dissecting microscope. The buds were immersed in lysis/binding solution (Ambion) on ice and were stored at –80°C until RNA extraction. The roots of seedlings were kept moist during sampling. Sampling was done between 11 AM to 2 PM during the day. Total RNA was extracted using the Trizol method (Life Technologies), and then separated on a denaturing glyoxal agarose gel and transferred to a Hybond membrane (Amersham Biosciences). Membranes were probed with SbTB1, SbDRM1, and SbUBQ (S. bicolor ubiquitin) genes. Probes were prepared by PCR amplification from a cDNA prepared from sorghum axillary buds using primers for SbTB1, forward 5'-GGTGGTGGTTCAAATGGTTC-3' and reverse 5'-TACAATGGCTCCTCAACACG-3'; for SbDRM1, forward 5'-TGGTGGCTTTGTGAGTGAAG-3' and reverse 5'-TTATCAGCAACAGCGACAGC-3'; and for SbUBQ, forward 5'-GGAAACATAGGGACGCTTCA-3' and reverse AAGGAGTCCACCCTTCACCT-3'. Northern hybridization was done at 65°C and washed with 0.1x SSPE or SSC and 0.5x SDS. Membranes were exposed to an imaging plate and analyzed using a phosphor imager. After subtracting background, the target mRNA photostimulated luminescence of each sample was divided by the corresponding ubiquitin mRNA photostimulated luminescence. The level of the control wild-type target mRNA at 7 DAP was adjusted to one, and comparable samples were adjusted by the same factor to provide relative abundance. Northern analyses were done at least twice from buds collected from a minimum of 25 seedlings grown at different times, and representative results are presented. Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers AF322132 (SbTB1) and CN135114 (SbDRM1).
T.H.K. thanks Dr. William Park for his helpful comments and discussions. Received November 29, 2005; returned for revision January 14, 2006; accepted January 15, 2006.
1 This work was supported by the Texas Agricultural Experiment Station.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Scott A. Finlayson (sfinlayson{at}tamu.edu). Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.074856. * Corresponding author; e-mail sfinlayson{at}tamu.edu; fax 979–845–0456.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1991) Gapped BLAST and PSI-BLAST: a new generation of protein database search program. Nucleic Acids Res 25: 3389–3402 Beall FD, Morgan PW, Mander LN, Miller FR, Babb KH (1991) Genetic regulation of development in Sorghum bicolor: V. The Boccalandro HE, Ploschuk EL, Yanovsky MJ, Sanchez RA, Gatz C, Casal JJ (2003) Increased phytochrome B alleviates density effects on tuber yield of field potato crops. Plant Physiol 133: 1539–1546 Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/MAX4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8: 443–449[CrossRef][ISI][Medline] Casal JJ, Sanchez RA, Deregibus VA (1986) The effect of plant density on tillering: the involvement of R/FR ratio and the proportion of radiation intercepted per plant. Environ Exp Bot 26: 365–371[CrossRef][ISI] Childs KL, Cordonnier-Pratt M-M, Pratt LH, Morgan PW (1992) Genetic regulation of development in Sorghum bicolor: VIII. Childs KL, Miller FR, Cordonnier-Pratt M-M, Pratt LH, Morgan PW, Mullet JE (1997) The sorghum photoperiod sensitivity gene, Ma3, encodes a phytochrome B. Plant Physiol 113: 611–619[Abstract] Cline MG (1997) Concepts and terminology of apical dominance. Am J Bot 84: 1064–1069[Abstract] Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18: 215–222[CrossRef][ISI][Medline] Devlin PF, Yanovsky MJ, Kay SA (2003) A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol 133: 1617–1629 Doebley J, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129: 285–295[Abstract] Doebley J, Stec A, Gustus C (1995) teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141: 333–346[Abstract] Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386: 385–388[CrossRef] Faivre-Rampant O, Bryan GJ, Roberts AG, Milbourne D, Viola R, Taylor MA (2004) Regulated expression of a novel TCP domain transcription factor indicates an involvement in the control of meristem activation processes in Solanum tuberosum. J Exp Bot 55: 951–953 Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17: 464–474 Gaudin V, Lunness PA, Fobert PR, Towers M, Riou-Khamlichi C, Murray JAH, Coen E, Doonan JH (2000) The expression of D-Cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea gene. Plant Physiol 122: 1137–1148 Greb T, Clarenz O, Schafer E, Muller D, Ruben H, Schmitz G, Theres K (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17: 1175–1187 Halliday KJ, Fankhauser C (2003) Phytochrome-hormonal signaling networks. New Phytol 157: 449–463[CrossRef][ISI] Hubbard L, McSteen P, Doebley J, Hake S (2002) Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte. Genetics 162: 1927–1935 Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46: 79–86 Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9: 1607–1619[Abstract] Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30: 337–348[CrossRef][ISI][Medline] Leyser HMO, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin resistant gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364: 161–164[CrossRef][Medline] Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 102: 12978–12983 Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, et al (2003) Control of tillering in rice. Nature 422: 618–621[CrossRef][Medline] Lukens L, Doebley J (2001) Molecular evolution of the teosinte branched gene among maize and related grasses. Mol Biol Evol 18: 627–638 Madoka Y, Mori H (2000) Two novel transcripts expressed in pea dormant axillary buds. Plant Cell Physiol 41: 274–281[ISI][Medline] Mathews S, Sharrock RA (1996) The phytochrome gene family in grasses (Poaceae): A phylogeny and evidence that grasses have a subset of the loci found in dicot angiosperms. Mol Biol Evol 13: 1141–1150[Abstract] McSteen P, Leyser O (2005) Shoot branching. Annu Rev Plant Biol 56: 353–374[CrossRef][Medline] Napoli CA, Beveridge CA, Snowden KC (1999) Reevaluating concepts of apical dominance and the control of axillary bud outgrowth. Curr Top Dev Biol 44: 127–169[ISI][Medline] Quail PH (2002) Phytochrome photosensory signaling networks. Nat Rev Mol Cell Biol 3: 85–93[CrossRef][ISI][Medline] Reed JW, Nagpal P, Poole DS, Furuya M, Chory J (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5: 147–157[Abstract] Sawers RJH, Sheehan MJ, Brutnell TP (2005) Cereal phytochromes: targets of selection, targets of manipulation? Trends Plant Sci 10: 138–143[ISI][Medline] Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K (1999) The Lateral suppressor (LS) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci USA 96: 290–295 Shimizu S, Mori H (2001) Control of outgrowth and dormancy in axillary buds. Plant Physiol 127: 1405–1413 Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucus HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17: 746–759 Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, Geiss G, McKhann H, Garcion C, Vaucheret H, Sandberg G, et al (2005) Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17: 1343–1359 Stafstrom JP (2000) Regulation of growth and dormancy in pea axillary buds. In JD Viemont, J Crabbe, eds, Dormancy in Plants. CAB International, Wallingford, UK, pp 331–346 Stafstrom JP, Krueger MT, Stoudt W (1998a) Nucleotide sequence of AtDRM1-1 cDNA and genomic clones (accession nos. AF053746 and AF053747), an Arabidopsis homologue of a pea dormant bud-associated gene. Plant Physiol 117: 718 Stafstrom JP, Ripley BD, Devitt ML, Drake B (1998b) Dormancy-associated gene expression in pea axillary buds. Planta 205: 547–552[CrossRef][ISI][Medline] Stirnberg P, Chatfield SP, Leyser HMO (1999) AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. Plant Physiol 121: 839–847 Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33: 513–520[CrossRef][ISI][Medline] Tanaka S-I, Nakamura S, Mochizuki N, Nagatani A (2002) Phytochrome in cotyledons regulates the expression of genes in the hypocotyl through auxin-dependent and -independent pathways. Plant Cell Physiol 43: 1171–1181 Tatematsu K, Ward S, Leyser O, Kamiya Y, Nambara E (2005) Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis. Plant Physiol 138: 757–766 Thimann KV, Skoog F (1933) Studies on the growth hormone of plants. III. The inhibiting action of the growth substance on bud development. Proc Natl Acad Sci USA 19: 714–716 Tremousaygue D, Garnier L, Bardet C, Dabos P, Harve C, Lescure B (2003) Internal telomeric repeats and ‘TCP domain’ protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells. Plant J 33: 957–966[CrossRef][ISI][Medline] Wan C, Sosebee RE (1998) Tillering responses to red:far-red light ratio during different phenological stages in Eragrostis curvula. Environ Exp Bot 40: 247–254[CrossRef][ISI] Ward SP, Leyser O (2004) Shoot branching. Curr Opin Plant Biol 7: 73–78[CrossRef][ISI][Medline] This article has been cited by other articles:
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allele results in gibberellin enrichment. Plant Physiol 95: 116–125
