In response to environmental changes, plants continuously make architectural changes in order to optimize their growth and development. The regulation of plant branching, influenced by environmental conditions and affecting hormone balance and gene expression, is crucial for agronomic purposes due to its direct correlation with yield. Strigolactones (SL), the youngest class of phytohormones, function to shape the architecture of plants by inhibiting axillary outgrowth. Barley plants harboring the mutation in the HvDWARF14 (HvD14) gene, which encodes the SL-specific receptor, produce almost twice as many tillers as wild-type (WT) Sebastian plants. Here, through hormone profiling and comparison of transcriptomic and proteomic changes between 2- and 4-week-old plants of WT and hvd14 genotypes, we elucidate a regulatory mechanism that might affect the tillering of SL-insensitive plants. The analysis showed statistically significant increased cytokinin content and decreased auxin and abscisic acid content in 'bushy' hvd14 compared to WT, which aligns with the commonly known actions of these hormones regarding branching regulation. Further, transcriptomic and proteomic analysis revealed a set of differentially expressed genes (DEG) and abundant proteins (DAP), among which 11.6% and 14.6% were associated with phytohormone-related processes, respectively. Bioinformatics analyses then identified a series of potential SL-dependent transcription factors (TF), which may control the differences observed in the hvd14 transcriptome and proteome. Comparison to available Arabidopsis thaliana data implicates a sub-selection of these TF as being involved in the transduction of SL signal in both monocotyledonous and dicotyledonous plants.

Department of Biological Sciences University of Alberta 11455 Saskatchewan Drive Edmonton AB T6G 2E9 Canada

Institute of Biology Biotechnology and Environmental Protection Faculty of Natural Sciences University of Silesia in Katowice Jagiellonska 28 40 032 Katowice Poland

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany The Czech Academy of Sciences Olomouc Czech Republic

Zobrazit více v PubMed

Aliche, E. B., Screpanti, C., De Mesmaeker, A., Munnik, T. & Bouwmeester, H. J. Science and application of strigolactones. New Phytol.227, 1001–1011 (2020). PubMed PMC

Wang, M. Molecular regulatory network of BRANCHED1 (BRC1) expression in axillary bud of Rpsa sp. in response to sugar and auxin. (Agrocampus Ouest, 2019).

Aguilar-Martínez, J. A., Poza-Carrión, C. & Cubas, P. Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. The Plant Cell19, 458–472 (2007). PubMed PMC

Mashiguchi, K. et al. Feedback-regulation of strigolactone biosynthetic genes and strigolactone-regulated genes in arabidopsis. Biosci. Biotechnol. Biochem.73, 2460–2465 (2009). PubMed

Braun, N. et al. The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol.158, 225–238 (2012). PubMed PMC

Dun, E. A., de Saint Germain, A., Rameau, C. & Beveridge, C. A. Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol.158, 487–498 (2012). PubMed PMC

Stes, E. et al. Strigolactones as an auxiliary hormonal defence mechanism against leafy gall syndrome in Arabidopsis thaliana. J. Exp. Botany66, 5123–5134 (2015). PubMed PMC

Muhr, M., Prüfer, N., Paulat, M. & Teichmann, T. Knockdown of strigolactone biosynthesis genes in Populus affects BRANCHED1 expression and shoot architecture. New Phytologist212, 613–626 (2016). PubMed

Soundappan, I. et al. SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in arabidopsis. Plant Cell27, 3143–3159 (2015). PubMed PMC

Wang, L. et al. Strigolactone signaling in arabidopsis regulates shoot development by targeting D53-Like SMXL repressor proteins for ubiquitination and degradation. Plant Cell27, 3128–3142 (2015). PubMed PMC

Song, X. et al. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res.27, 1128–1141 (2017). PubMed PMC

Skoog, F. & Thimann, K. V. Further experiments on the inhibition of the development of lateral buds by growth hormone. Proc. Natl. Acad. Sci. USA20, 480–485 (1934). PubMed PMC

Snow, R. On the upward inhibiting effect of auxin in shoots. The New Phytologist37, 173–185 (1938).

Cline, M. G. Exogenous auxin effects on lateral bud outgrowth in decapitated shoots. Ann. Botany78, 255–266 (1996).

Müller, D. & Leyser, O. Auxin, cytokinin and the control of shoot branching. Ann. Botany107, 1203–1212 (2011). PubMed PMC

Adamowski, M. & Friml, J. PIN-dependent auxin transport: action, regulation, and evolution. The Plant Cell27, 20–32 (2015). PubMed PMC

Bennett, T. et al. The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr. Biol.16, 553–563 (2006). PubMed

Arite, T. et al. DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J.51, 1019–1029 (2007). PubMed

Shinohara, N., Taylor, C. & Leyser, O. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin Efflux Protein PIN1 from the plasma membrane. PLOS Biol.11, e1001474 (2013). PubMed PMC

Crawford, S. et al. Strigolactones enhance competition between shoot branches by dampening auxin transport. Development137, 2905–2913 (2010). PubMed

Hayward, A., Stirnberg, P., Beveridge, C. & Leyser, O. Interactions between Auxin and Strigolactone in Shoot Branching Control. Plant Physiol.151, 400–412 (2009). PubMed PMC

Foo, E. et al. The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell17, 464–474 (2005). PubMed PMC

Johnson, X. et al. Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol.142, 1014–1026 (2006). PubMed PMC

Sorefan, K. et al. MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev.17, 1469–1474 (2003). PubMed PMC

Fichtner, F. et al. Trehalose 6-phosphate is involved in triggering axillary bud outgrowth in garden pea (Pisum sativum L.). The Plant J.92, 611–623 (2017). PubMed

Dierck, R. et al. Change in auxin and cytokinin levels coincides with altered expression of branching genes during axillary bud outgrowth in chrysanthemum. PLOS One11, e0161732 (2016). PubMed PMC

Minakuchi, K. et al. FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol.51, 1127–1135 (2010). PubMed PMC

Helliwell, C. A. et al. The arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. The Plant Cell13, 2115–2125 (2001). PubMed PMC

Chen, S. et al. The transcription factor SPL13 mediates strigolactone suppression of shoot branching by inhibiting cytokinin synthesis in Solanum lycopersicum. J. Exp. Botany74, 5722–5735 (2023). PubMed PMC

Tanaka, M., Takei, K., Kojima, M., Sakakibara, H. & Mori, H. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. The Plant J.45, 1028–1036 (2006). PubMed

Marzec, M., Gruszka, D., Tylec, P. & Szarejko, I. Identification and functional analysis of the HvD14 gene involved in strigolactone signaling in Hordeum vulgare. Physiol. Plantarum.158, 341–355 (2016). PubMed

Daszkowska-Golec, A. et al. Multi-omics insights into the positive role of strigolactone perception in barley drought response. BMC Plant Biol.23, 445 (2023). PubMed PMC

Xu, P., Chen, H. & Cai, W. Transcription factor CDF4 promotes leaf senescence and floral organ abscission by regulating abscisic acid and reactive oxygen species pathways in Arabidopsis. EMBO Rep.21, e48967 (2020). PubMed PMC

Noguero, M., Atif, R. M., Ochatt, S. & Thompson, R. D. The role of the DNA-binding one zinc finger (DOF) transcription factor family in plants. Plant Sci.209, 32–45 (2013). PubMed

Kang, H.-G. & Singh, K. B. Characterization of salicylic acid-responsive, Arabidopsis Dof domain proteins: Overexpression of OBP3 leads to growth defects. The Plant J.21, 329–339 (2000). PubMed

Jha, P. & Kumar, V. BABY BOOM (BBM): A candidate transcription factor gene in plant biotechnology. Biotechnol. Lett.40, 1467–1475 (2018). PubMed

Scheres, B. & Krizek, B. A. Coordination of growth in root and shoot apices by AIL/PLT transcription factors. Curr. Opin. Plant Biol.41, 95–101 (2018). PubMed

Galinha, C. et al. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature449, 1053–1057 (2007). PubMed

Li, M. et al. Auxin biosynthesis maintains embryo identity and growth during BABY BOOM-induced somatic embryogenesis. Plant Physiol.188, 1095–1110 (2022). PubMed PMC

Boutilier, K. et al. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. The Plant Cell14, 1737–1749 (2002). PubMed PMC

Bowman, J. L. & Moyroud, E. Reflections on the ABC model of flower development. The Plant Cell36, 1334. 10.1093/plcell/koae044 (2024). PubMed PMC

Wang, L. et al. Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature583, 277–281 (2020). PubMed

Assuero, S. G. & Tognetti, J. A. Tillering regulation by endogenous and environmental factors and its agricultural management. Am. J. Plant Sci. Biotechnol.4, 35–48 (2010).

Hussien, A. et al. Genetics of Tillering in Rice and Barley. The Plant Genome7, plantgenome2013.10.0032 (2014).

Dun, E. A., Brewer, P. B., Gillam, E. M. J. & Beveridge, C. A. Strigolactones and shoot branching: What Is the real hormone and how does it work?. Plant Cell Physiol.64, 967–983 (2023). PubMed PMC

Korek, M., Uhrig, R. G. & Marzec, M. Strigolactone insensitivity affects differential shoot and root transcriptome in barley. J. Appl. Genetics10.1007/s13353-024-00885-w (2024). PubMed PMC

Altmann, M. et al. Extensive signal integration by the phytohormone protein network. Nature583, 271–276 (2020). PubMed

Yao, C. & Finlayson, S. A. Abscisic acid is a general negative regulator of arabidopsis axillary bud growth1[OPEN]. Plant Physiol.169, 611–626 (2015). PubMed PMC

González-Grandío, E. et al. Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds. Proc. Natl. Acad. Sci.114, E245–E254 (2017). PubMed PMC

Cheng, Y. et al. Jasmonic acid negatively regulates branch growth in pear. Front. Plant Sci.14, (2023). PubMed PMC

Hong, S.-Y. et al. Heterologous microProtein expression identifies LITTLE NINJA, a dominant regulator of jasmonic acid signaling. Proc. Natl. Acad. Sci.117, 26197–26205 (2020). PubMed PMC

Shimizu-Sato, S., Tanaka, M. & Mori, H. Auxin–cytokinin interactions in the control of shoot branching. Plant Mol. Biol.69, 429–435 (2009). PubMed

Balla, J., Kalousek, P., Reinöhl, V., Friml, J. & Procházka, S. Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. The Plant J.65, 571–577 (2011). PubMed

Xu, J. et al. The interaction between nitrogen availability and auxin, cytokinin, and strigolactone in the control of shoot branching in rice (Oryza sativa L.). Plant Cell Rep.34, 1647–1662 (2015). PubMed

Wani, A. B., Chadar, H., Wani, A. H., Singh, S. & Upadhyay, N. Salicylic acid to decrease plant stress. Environ. Chem. Lett.15, 101–123 (2017).

Abdelkader, M. & Hamad,. Response of growth, yield and chemical constituents of Roselle plant to foliar application of Ascorbic Acid and Salicylic Acid. Glob. J. Agric. Food Saf. Sci.1, 126–136 (2014).

Abou El-Yazeid, A. Effect of foliar application of salicylic acid and chelated zinc on growth and productivity of sweet pepper (Capsicum annuum L.) under autumn planting. Res. J. Agric. Biol. Sci., 423–433 (2011).

Hesami, S., Nabizadeh, E., Rahimi, A. & Rokhzadi, A. Effects of salicylic acid levels and irrigation intervals on growth and yield of coriander (Coriandrum sativum) in field conditions.

Li, L. et al. Protein degradation rate in arabidopsis thaliana leaf growth and development. The Plant Cell29, 207–228 (2017). PubMed PMC

Creelman, R. A., Bell, E. & Mullet, J. E. Involvement of a lipoxygenase-like enzyme in abscisic acid biosynthesis 1. Plant Physiol.99, 1258–1260 (1992). PubMed PMC

Korek, M. & Marzec, M. Strigolactones and abscisic acid interactions affect plant development and response to abiotic stresses. BMC Plant Biol.23, 314 (2023). PubMed PMC

Marzec, M. et al. Barley strigolactone signalling mutant hvd14.d reveals the role of strigolactones in abscisic acid-dependent response to drought. Plant Cell Environ.43, 2239–2253 (2020). PubMed

van Es, S. W. et al. A gene regulatory network critical for axillary bud dormancy directly controlled by Arabidopsis BRANCHED1. New Phytologist241, 1193–1209 (2024). PubMed

Wasternack, C. & Hause, B. Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development An update to the 2007 review in Annals of Botany. Ann. Botany111, 1021–1058 (2013). PubMed PMC

Viswanath, K. K. et al. Plant lipoxygenases and their role in plant physiology. J. Plant Biol.63, 83–95 (2020).

Bell, E., Creelman, R. A. & Mullet, J. E. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc. Natl. Acad. Sci.92, 8675–8679 (1995). PubMed PMC

Lim, C. W. et al. The pepper lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response. Plant Cell Physiol.56, 930–942 (2015). PubMed

Hou, S., Lin, L., Lv, Y., Xu, N. & Sun, X. Responses of lipoxygenase, jasmonic acid, and salicylic acid to temperature and exogenous phytohormone treatments in Gracilariopsis lemaneiformis (Rhodophyta). J. Appl. Phycol.30, 3387–3394 (2018).

Bhardwaj, P. K., Kaur, J., Sobti, R. C., Ahuja, P. S. & Kumar, S. Lipoxygenase in Caragana jubata responds to low temperature, abscisic acid, methyl jasmonate and salicylic acid. Gene483, 49–53 (2011). PubMed

Melan, M. A. et al. An arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiol.101, 441–450 (1993). PubMed PMC

Gaillochet, C. et al. A molecular network for functional versatility of HECATE transcription factors. The Plant J.95, 57–70 (2018). PubMed

Zhu, K. et al. Ethylene activation of carotenoid biosynthesis by a novel transcription factor CsERF061. J. Exp. Botany72, 3137–3154 (2021). PubMed

Shanks, C. M. et al. Role of BASIC PENTACYSTEINE transcription factors in a subset of cytokinin signaling responses. Plant J.95, 458–473 (2018). PubMed

Pruneda-Paz, J. L., Breton, G., Para, A. & Kay, S. A. A functional genomics approach reveals CHE as a component of the arabidopsis circadian clock. Science323, 1481–1485 (2009). PubMed PMC

Robertson, F. C., Skeffington, A. W., Gardner, M. J. & Webb, A. A. R. Interactions between circadian and hormonal signalling in plants. Plant Mol. Biol.69, 419–427 (2009). PubMed

Wang, F. et al. The rice circadian clock regulates tiller growth and panicle development through strigolactone signaling and sugar sensing. Plant Cell32, 3124–3138 (2020). PubMed PMC

Guo, Y., Qin, G., Gu, H. & Qu, L.-J. Dof5.6/HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in arabidopsis. The Plant Cell21, 3518–3534 (2009). PubMed PMC

Agusti, J. et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl. Acad. Sci.108, 20242–20247 (2011). PubMed PMC

Yin, Y. et al. A new class of transcription factors mediates brassinosteroid-regulated gene expression in arabidopsis. Cell120, 249–259 (2005). PubMed

Hu, J., Ji, Y., Hu, X., Sun, S. & Wang, X. BES1 functions as the Co-regulator of D53-like SMXLs to Inhibit BRC1 expression in strigolactone-regulated shoot branching in arabidopsis. Plant Commun.1, 100014 (2019). PubMed PMC

Liu, X. et al. A multifaceted module of BRI1 ETHYLMETHANE SULFONATE SUPRESSOR1 (BES1)-MYB88 in growth and stress tolerance of apple. Plant Physiol.185, 1903–1923 (2021). PubMed PMC

Šimura, J. et al. Plant hormonomics: Multiple phytohormone profiling by targeted metabolomics. Plant Physiol.177, 476–489 (2018). PubMed PMC

Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol.34, 525–527 (2016). PubMed

Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol.15, 550 (2014). PubMed PMC

Leutert, M., Rodríguez-Mias, R. A., Fukuda, N. K. & Villén, J. R2–P2 rapid-robotic phosphoproteomics enables multidimensional cell signaling studies. Mol. Syst. Biol.15, e9021 (2019). PubMed PMC

Tyanova, S., Temu, T. & Cox, J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat. Protoc.11, 2301–2319 (2016). PubMed

Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods13, 731–740 (2016). PubMed