Bioinformatic insights into sugar signaling pathways in sugarcane growth.
Bioinformatics
Carbohydrates
Hexokinase
SnRK1
Sugar signaling kinases
TOR
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
22 10 2024
22 10 2024
Historique:
received:
07
05
2024
accepted:
03
10
2024
medline:
23
10
2024
pubmed:
23
10
2024
entrez:
22
10
2024
Statut:
epublish
Résumé
The SnRK1, hexokinase, and TORC1 (TOR, LST8, RAPTOR) are three pivotal kinases at the core of sugar level sensing, significantly impacting plant metabolism and development. We retrieved and analyzed protein sequences of these three kinase pathways from seven sugarcane transcriptome and genome datasets, identifying protein domains, phylogenetic relationships, sequence ancestry, and in silico expression levels. Additionally, we predicted HXK subcellular localization and assessed its enzymatic activity in sugarcane leaves and culms along development in the field. We retrieved 11 TOR, 23 RAPTOR, 55 LST8, 95 SnRK1α, 98 HXK, and 14 HXK-like putative full-length sequences containing all the conserved domains. Most of these transcripts seem to share a common origin with the three ancestral species of sugarcane: Saccharum officinarum, Saccharum spontaneum, and Saccharum barberi. We accessed the expression profile of sequences from one sugarcane transcriptome. We found the highest enzymatic activity of HXK in culms in the first month, which, at this stage, provides carbon (sucrose) and nitrogen (amino acids) for initial plant development. Our approach places novel sugar sensing sequences that work as a guideline for further research into the underlying signaling mechanisms and biotechnology applications in sugarcane.
Identifiants
pubmed: 39438542
doi: 10.1038/s41598-024-75220-8
pii: 10.1038/s41598-024-75220-8
doi:
Substances chimiques
Plant Proteins
0
Sugars
0
Hexokinase
EC 2.7.1.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
24935Subventions
Organisme : Research Center of Green House Gas Innovation (RCGI)
ID : (FAPESP 2014/50279-4; 2020/15230-5)
Organisme : National Institute of Bioethanol Science and Technology - INCT of Bioethanol
ID : (FAPESP 2014/50884-5; CNPq 465319/2014-9)
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 142090/2018-2
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 310080/2018-5
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 115313/2019-2
Organisme : Research Center of Green House Gas Innovation
ID : 371055
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : 2022/00441-6
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : 2018/03764-5
Informations de copyright
© 2024. The Author(s).
Références
FAO. The State of Food and Agriculture (FAO, Rome, 2021).
Margalha, L., Confraria, A. & Baena-González, E. SnRK1 and TOR: modulating growth-defense trade-offs in plant stress responses. J. Exp. Bot. 70, 2261–2274 (2019).
pubmed: 30793201
doi: 10.1093/jxb/erz066
Baena-González, E. & Hanson, J. Shaping plant development through the SnRK1-TOR metabolic regulators. Curr. Opin. Plant Biol. 35, 152–157 (2017).
pubmed: 28027512
doi: 10.1016/j.pbi.2016.12.004
Wu, Y. et al. Integration of nutrient, energy, light, and hormone signalling via TOR in plants. J. Exp. Bot. 70, 2227–2238 (2019).
pubmed: 30715492
pmcid: 6463029
doi: 10.1093/jxb/erz028
Li, L., Liu, K.-H. & Sheen, J. Dynamic nutrient signaling networks in plants. Annu. Rev. Cell Dev. Biol. 37, 341–367 (2021).
pubmed: 34351784
pmcid: 8497281
doi: 10.1146/annurev-cellbio-010521-015047
Nukarinen, E. et al. Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation. Sci. Rep. 6, 31697 (2016).
pubmed: 27545962
pmcid: 4992866
doi: 10.1038/srep31697
Van Leene, J. et al. Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase. Nat. Plants 5, 316–327 (2019).
pubmed: 30833711
doi: 10.1038/s41477-019-0378-z
Henriques, R., Bögre, L., Horváth, B. & Magyar, Z. Balancing act: matching growth with environment by the TOR signalling pathway. J. Exp. Bot. 65, 2691–2701 (2014).
pubmed: 24567496
doi: 10.1093/jxb/eru049
Dobrenel, T. et al. TOR Signaling and Nutrient Sensing. Annu. Rev. Plant Biol. 67, 261–285 (2016).
pubmed: 26905651
doi: 10.1146/annurev-arplant-043014-114648
González, A. & Hall, M. N. Nutrient sensing and TOR signaling in yeast and mammals. EMBO J. 36, 397–408 (2017).
pubmed: 28096180
pmcid: 5694944
doi: 10.15252/embj.201696010
Menand, B. et al. Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene. Proc. Natl. Acad. Sci. 99, 6422–6427 (2002).
pubmed: 11983923
pmcid: 122964
doi: 10.1073/pnas.092141899
Moreau, M. et al. Mutations in the Arabidopsis homolog of LST8/GbetaL, a partner of the target of Rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24, 463–481 (2012).
pubmed: 22307851
pmcid: 3315227
doi: 10.1105/tpc.111.091306
Kim, D.-H. et al. GβL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between Raptor and mTOR. Mol. Cell 11, 895–904 (2003).
pubmed: 12718876
doi: 10.1016/S1097-2765(03)00114-X
Anderson, G. H., Veit, B. & Hanson, M. R. The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biol. 3, 12 (2005).
pubmed: 15845148
pmcid: 1131892
doi: 10.1186/1741-7007-3-12
Deprost, D., Truong, H.-N., Robaglia, C. & Meyer, C. An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem. Biophys. Res. Commun. 326, 844–850 (2005).
pubmed: 15607746
doi: 10.1016/j.bbrc.2004.11.117
Maegawa, K., Takii, R., Ushimaru, T. & Kozaki, A. Evolutionary conservation of TORC1 components, TOR, Raptor, and LST8, between rice and yeast. Mol. Genet. Genomics MGG 290, 2019–2030 (2015).
pubmed: 25956502
doi: 10.1007/s00438-015-1056-0
Baena-González, E., Rolland, F., Thevelein, J. M. & Sheen, J. A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938–942 (2007).
pubmed: 17671505
doi: 10.1038/nature06069
Broeckx, T., Hulsmans, S. & Rolland, F. The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function. J. Exp. Bot. 67, 6215–6252 (2016).
pubmed: 27856705
doi: 10.1093/jxb/erw416
Rodriguez, M., Parola, R., Andreola, S., Pereyra, C. & Martínez-Noël, G. TOR and SnRK1 signaling pathways in plant response to abiotic stresses: Do they always act according to the “yin-yang” model?. Plant Sci. 288, 110220 (2019).
pubmed: 31521220
doi: 10.1016/j.plantsci.2019.110220
Emanuelle, S., Doblin, M. S., Gooley, P. R. & Gentry, M. S. The UBA domain of SnRK1 promotes activation and maintains catalytic activity. Biochem. Biophys. Res. Commun. 497, 127–132 (2018).
pubmed: 29428737
pmcid: 6463285
doi: 10.1016/j.bbrc.2018.02.039
Sugden, C., Crawford, R. M., Halford, N. G. & Hardie, D. G. Regulation of spinach SNF1-related (SnRK1) kinases by protein kinases and phosphatases is associated with phosphorylation of the T loop and is regulated by 5 ’-AMP. Plant J. 19, 433–439 (1999).
pubmed: 10504565
doi: 10.1046/j.1365-313X.1999.00532.x
Jang, J. C. & Sheen, J. Sugar sensing in higher plants. Trends Plant Sci. 2, 208–213 (1997).
doi: 10.1016/S1360-1385(97)89545-3
Moore, B. et al. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300, 332–336 (2003).
pubmed: 12690200
doi: 10.1126/science.1080585
Cho, J.-I. et al. Structure, expression, and functional analysis of the hexokinase gene family in rice (Oryza sativa L.). Planta 224, 598–611 (2006).
pubmed: 16552590
doi: 10.1007/s00425-006-0251-y
Zhang, Z. et al. Isolation, structural analysis, and expression characteristics of the maize (Zea mays L.) hexokinase gene family. Mol. Biol. Rep. 41, 6157–6166 (2014).
pubmed: 24962048
doi: 10.1007/s11033-014-3495-9
Sheen, J. Master regulators in plant glucose signaling networks. J. Plant Biol. Singmul Hakhoe Chi 57, 67–79 (2014).
pubmed: 25530701
Aguilera-Alvarado, G. P. & Sánchez-Nieto, S. Plant Hexokinases are multifaceted proteins. Plant Cell Physiol. 58, 1151–1160 (2017).
pubmed: 28449056
doi: 10.1093/pcp/pcx062
Moore, P. H. Temporal and spatial regulation of sucrose accumulation in the sugarcane stem. Aust. J. Plant Physiol. 22, 661–679 (1995).
Grandis, A., Fortirer, J. S., Navarro, B. V., de Oliveira, L. P. & Buckeridge, M. S. Biotechnologies to improve sugarcane productivity in a climate change scenario. BioEnergy Res. 17, 1–26 (2024).
doi: 10.1007/s12155-023-10649-9
De Souza, A. P., Grandis, A., Arenque-Musa, B. C. & Buckeridge, M. S. Diurnal variation in gas exchange and nonstructural carbohydrates throughout sugarcane development. Funct. Plant Biol. 45, 865–876 (2018).
pubmed: 32291068
doi: 10.1071/FP17268
Rohwer, J. M. & Botha, F. C. Analysis of sucrose accumulation in the sugar cane culm on the basis of in vitro kinetic data. Biochem. J. 358, 437–445 (2001).
pubmed: 11513743
pmcid: 1222077
doi: 10.1042/bj3580437
Welbaum, G. E. & Meinzer, F. C. Compartmentation of solutes and water in developing sugarcane stalk tissue. Plant Physiol. 93, 1147–1153 (1990).
pubmed: 16667571
pmcid: 1062644
doi: 10.1104/pp.93.3.1147
De Souza, A. P. et al. Elevated CO2 increases photosynthesis, biomass and productivity, and modifies gene expression in sugarcane. Plant Cell Environ. 31, 1116–1127 (2008).
pubmed: 18433443
doi: 10.1111/j.1365-3040.2008.01822.x
Huerta-Cepas, J. et al. A hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 44, D286–D293 (2016).
pubmed: 26582926
doi: 10.1093/nar/gkv1248
Huerta-Cepas, J. et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, 309–314 (2019).
doi: 10.1093/nar/gky1085
de Oliveira, L. P. et al. Bioinformatic analyses to uncover genes involved in trehalose metabolism in the polyploid sugarcane. Sci. Rep. 12, (2022).
Robaglia, C., Thomas, M. & Meyer, C. Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr. Opin. Plant Biol. 15, 301–307 (2012).
pubmed: 22305521
doi: 10.1016/j.pbi.2012.01.012
Vettore, A. L. et al. Analysis and functional annotation of an expressed sequence tag collection for tropical crop sugarcane. Genome Res. 13, 2725–2735 (2003).
pubmed: 14613979
pmcid: 403815
doi: 10.1101/gr.1532103
Mattiello, L. et al. Physiological and transcriptional analyses of developmental stages along sugarcane leaf. BMC Plant Biol. 15, 300 (2015).
pubmed: 26714767
pmcid: 4696237
doi: 10.1186/s12870-015-0694-z
Riaño-Pachón, D. M. & Mattiello, L. Draft genome sequencing of the sugarcane hybrid SP80–3280. F1000Research 6, 861 (2017).
pubmed: 28713559
pmcid: 5499785
doi: 10.12688/f1000research.11859.2
Hoang, N. V. et al. A survey of the complex transcriptome from the highly polyploid sugarcane genome using full-length isoform sequencing and de novo assembly from short read sequencing. BMC Genom. 18, 395 (2017).
doi: 10.1186/s12864-017-3757-8
Garsmeur, O. et al. A mosaic monoploid reference sequence for the highly complex genome of sugarcane. Nat. Commun. 9, (2018).
Zhang, J. et al. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat. Genet.Bold">50, 1565–1573 (2018).
pubmed: 30297971
doi: 10.1038/s41588-018-0237-2
Souza, G. M. et al. Assembly of the 373k gene space of the polyploid sugarcane genome reveals reservoirs of functional diversity in the world’s leading biomass crop. GigaScience 8, 1–18 (2019).
doi: 10.1093/gigascience/giz129
Zhou, M.-L. et al. Trehalose metabolism-related genes in maize. J. Plant Growth Regul. 33, 256–271 (2014).
doi: 10.1007/s00344-013-9368-y
Wang, J. et al. Characteristics, expression pattern and intracellular localisation of sugarcane cytoplasmic hexokinase gene ShHXK8. Sugar Tech 21, 909–916 (2019).
doi: 10.1007/s12355-019-00731-y
Gibon, Y. et al. A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16, 3304–3325 (2004).
pubmed: 15548738
pmcid: 535875
doi: 10.1105/tpc.104.025973
Wang, J., Zhao, T., Yang, B. & Zhang, S. Sucrose metabolism and regulation in sugarcane. J. Plant Physiol. Pathol. 2017, (2018).
Atanasov, V., Fürtauer, L. & Nägele, T. Indications for a central role of hexokinase activity in natural variation of heat acclimation in Arabidopsis thaliana. . Plants https://doi.org/10.20944/preprints202006.0169.v1 (2020).
doi: 10.20944/preprints202006.0169.v1
pubmed: 32610673
pmcid: 7411702
Lemoine, R. et al. Source-to-sink transport of sugar and regulation by environmental factors. Front. Plant Sci. 4 (2013).
Yoon, J., Cho, L.-H., Tun, W., Jeon, J.-S., & An, G. Sucrose signaling in higher plants. Plant Sci. Int. J. Exp. Plant Biol. 302, 110703 (2021).
Zeeman, S. C., Kossmann, J. & Smith, A. M. Starch: its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol. 61, 209–234 (2010).
pubmed: 20192737
doi: 10.1146/annurev-arplant-042809-112301
Peixoto, B. et al. Impact of the SnRK1 protein kinase on sucrose homeostasis and the transcriptome during the diel cycle. Plant Physiol. 187, 1357–1373 (2021).
pubmed: 34618060
pmcid: 8566312
doi: 10.1093/plphys/kiab350
Halford, N. G. & Hey, S. J. Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem. J. 419, 247–259 (2009).
pubmed: 19309312
doi: 10.1042/BJ20082408
Caldana, C., Martins, M. C. M., Mubeen, U. & Urrea-Castellanos, R. The magic ‘hammer’ of TOR: the multiple faces of a single pathway in the metabolic regulation of plant growth and development. J. Exp. Bot. 70, 2217–2225 (2019).
pubmed: 30722050
doi: 10.1093/jxb/ery459
Kelly, G. et al. Guard-cell hexokinase increases water-use efficiency under normal and drought conditions. Front. Plant Sci. 10, 1499 (2019).
pubmed: 31803219
pmcid: 6877735
doi: 10.3389/fpls.2019.01499
O’Leary, B. M., Oh, G. G. K., Lee, C. P. & Millar, A. H. Metabolite regulatory interactions control plant respiratory metabolism via target of rapamycin (TOR) Kinase activation([OPEN]). Plant Cell 32, 666–682 (2020).
pubmed: 31888967
doi: 10.1105/tpc.19.00157
Salazar-Díaz, K. et al. TOR senses and regulates spermidine metabolism during seedling establishment and growth in maize and Arabidopsis. iScience 24, 103260 (2021).
pubmed: 34765910
pmcid: 8571727
doi: 10.1016/j.isci.2021.103260
Wingler, A. Transitioning to the next phase: the role of sugar signaling throughout the plant life cycle. Plant Physiol. 176, 1075–1084 (2018).
pubmed: 28974627
doi: 10.1104/pp.17.01229
Carraro, D. M., Lambais, M. R. & Carrer, H. In silico characterization and expression analyses of sugarcane putative sucrose non-fermenting-1 (SNF1) related kinases. Genet. Mol. Biol. 24, 35–41 (2001).
doi: 10.1590/S1415-47572001000100006
de Maria Felix, J. et al. Expression profile of signal transduction components in a sugarcane population segregating for sugar content. Trop. Plant Biol.Bold">2, 98–109 (2009).
doi: 10.1007/s12042-009-9031-8
Papini-Terzi, F. S. et al. Sugarcane genes associated with sucrose content. BMC Genom. 10, 120 (2009).
doi: 10.1186/1471-2164-10-120
Zhao, T. et al. Structure, intracellular localisation and expression analysis of sucrose nonfermenting-related kinase ShSnRK1α in sugarcane. Sugar Tech 25, 69–76 (2023).
doi: 10.1007/s12355-022-01203-6
Hoepfner, S. W. & Botha, F. C. Purification and characterisation of fructokinase from the culm of sugarcane. Plant Sci. 167, 645–654 (2004).
doi: 10.1016/j.plantsci.2004.05.020
Vilela, M. de M. et al. Analysis of three sugarcane homo/homeologous regions suggests independent polyploidization events of Saccharum officinarum and Saccharum spontaneum. Genome Biol. Evol. 9, 266–278 (2017).
Cursi, D. E. et al. History and current status of sugarcane breeding, germplasm development and molecular genetics in brazil. Sugar Tech 24, 112–133 (2022).
doi: 10.1007/s12355-021-00951-1
Jackson, P. A. Breeding for improved sugar content in sugarcane. Field Crops Res. 92, 277–290 (2005).
doi: 10.1016/j.fcr.2005.01.024
Carneiro, A. E. V., Trivelin, P. C. O. & Victoria, R. L. Utilização da reserva orgânica e de nitrogênio do tolete de plantio (colmo-semente) no desenvolvimento da cana-planta. Sci. Agric. 52, 199–209 (1995).
doi: 10.1590/S0103-90161995000200001
Glasziou, K. T. The physiology of sugar-cane I. Studies on the nutritional and physiological interrelationships of the germinating cutting. Aust. J. Biol. Sci. 11, 16–16 (1958).
doi: 10.1071/BI9580016
Verma, A. K., Agarwal, A. K., Dubey, R. S., Solomon, S. & Singh, S. B. Sugar partitioning in sprouting lateral bud and shoot development of sugarcane. Plant Physiol. Biochem. 62, 111–115 (2013).
pubmed: 23208305
doi: 10.1016/j.plaphy.2012.10.021
Dong, P. et al. Expression profiling and functional analysis reveals that TOR is a key player in regulating photosynthesis and phytohormone signaling pathways in Arabidopsis. Front. Plant Sci. 6, 677 (2015).
pubmed: 26442001
pmcid: 4561354
doi: 10.3389/fpls.2015.00677
Song, Y., Alyafei, M. S., Masmoudi, K., Jaleel, A. & Ren, M. Contributions of TOR signaling on photosynthesis. Int. J. Mol. Sci. 22, 8959 (2021).
pubmed: 34445664
pmcid: 8396432
doi: 10.3390/ijms22168959
Upadhyaya, S. & Rao, B. J. Reciprocal regulation of photosynthesis and mitochondrial respiration by TOR kinase in Chlamydomonas reinhardtii. Plant Direct 3, e00184 (2019).
pubmed: 31832599
pmcid: 6854518
doi: 10.1002/pld3.184
Yang, H. et al. Mechanisms of mTORC1 activation by RHEB and inhibition by PRAS40. NatureBold">552, 368–373 (2017).
pubmed: 29236692
pmcid: 5750076
doi: 10.1038/nature25023
Smith, T. F., Gaitatzes, C., Saxena, K. & Neer, E. J. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24, 181–185 (1999).
pubmed: 10322433
doi: 10.1016/S0968-0004(99)01384-5
Jain, B. P. & Pandey, S. WD40 repeat proteins: signalling scaffold with diverse functions. Protein J. 37, 391–406 (2018).
pubmed: 30069656
doi: 10.1007/s10930-018-9785-7
Finn, R. D. et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44, D279-285 (2016).
pubmed: 26673716
doi: 10.1093/nar/gkv1344
Lo Conte, L. et al. SCOP: A structural classification of proteins database. Nucleic Acids Res. 28, 257–259 (2000).
pubmed: 10592240
pmcid: 102479
doi: 10.1093/nar/28.1.257
The SUPERFAMILY 1.75 database in 2014: a doubling of data. Abstract - Europe PMC. http://europepmc.org/article/PMC/4383889 .
Baena-González, E. & Lunn, J. E. SnRK1 and trehalose 6-phosphate—two ancient pathways converge to regulate plant metabolism and growth. Curr. Opin. Plant Biol. 55, 52–59 (2020).
pubmed: 32259743
doi: 10.1016/j.pbi.2020.01.010
Zhang, Y. et al. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol. 149, 1860–1871 (2009).
pubmed: 19193861
pmcid: 2663748
doi: 10.1104/pp.108.133934
Wu, L. G. & Birch, R. G. Physiological basis for enhanced sucrose accumulation in an engineered sugarcane cell line. Funct. Plant Biol. 37, 1161–1174 (2010).
doi: 10.1071/FP10055
Rodríguez-Saavedra, C. et al. Moonlighting proteins: the case of the hexokinases. Front. Mol. Biosci. 8, 701975 (2021).
pubmed: 34235183
pmcid: 8256278
doi: 10.3389/fmolb.2021.701975
Geng, M.-T. et al. Structure, expression, and functional analysis of the hexokinase gene family in Cassava. Int. J. Mol. Sci. 18, 1041 (2017).
pubmed: 28498327
pmcid: 5454953
doi: 10.3390/ijms18051041
Karve, A. et al. Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta 228, 411–425 (2008).
pubmed: 18481082
pmcid: 2953952
doi: 10.1007/s00425-008-0746-9
Aguilera-Alvarado, G. P., Guevara-García, Á. A., Estrada-Antolín, S. A. & Sánchez-Nieto, S. Biochemical properties and subcellular localization of six members of the HXK family in maize and its metabolic contribution to embryo germination. BMC Plant Biol. 19, 27 (2019).
pubmed: 30646852
pmcid: 6332545
doi: 10.1186/s12870-018-1605-x
Cho, J.-I. et al. Role of the rice hexokinases OsHXK5 and OsHXK6 as glucose sensors. Plant Physiol. 149, 745–759 (2009).
pubmed: 19010999
pmcid: 2633841
doi: 10.1104/pp.108.131227
Boussiengui-Boussiengui, G., Groenewald, J.-H. & Botha, F. C. Metabolic changes associated with the sink-source transition during sprouting of the axillary buds on the sugarcane culm. Trop. Plant Biol.Bold">1, 1–11 (2016).
doi: 10.1007/s12042-015-9158-8
Rae, A. L., Martinelli, A. P. & Dornelas, M. C. Anatomy and Morphology. In Sugarcane: Physiology, Biochemistry, and Functional Biology 19–34 (Wiley, Hoboken, 2013). https://doi.org/10.1002/9781118771280.ch2 .
Zhang, M. et al. Phosphomannose isomerase affects the key enzymes of glycolysis and sucrose metabolism in transgenic sugarcane overexpressing the manA gene. Mol. Breed. 35, 100 (2015).
pubmed: 25798049
doi: 10.1007/s11032-015-0295-4
Li, X. et al. Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes. Proc. Natl. Acad. Sci. U. S. A. 114, 2765–2770 (2017).
pubmed: 28223530
pmcid: 5347562
doi: 10.1073/pnas.1618782114
Pfeiffer, A. et al. Integration of light and metabolic signals for stem cell activation at the shoot apical meristem. eLife 5, e17023 (2016).
pubmed: 27400267
pmcid: 4969040
doi: 10.7554/eLife.17023
Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European molecular biology open software suite. Trends Genet. TIG 16, 276–277 (2000).
pubmed: 10827456
doi: 10.1016/S0168-9525(00)02024-2
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430
doi: 10.1093/molbev/msu300
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
pubmed: 20525638
doi: 10.1093/sysbio/syq010
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).
pubmed: 29077904
doi: 10.1093/molbev/msx281
Eddy, S. R. Profile hidden Markov models. Bioinformatics 14, 755–763 (1998).
pubmed: 9918945
doi: 10.1093/bioinformatics/14.9.755
Potter, S. C. et al. HMMER web server: 2018 update. Nucleic Acids Res. 46, W200–W204 (2018).
pubmed: 29905871
pmcid: 6030962
doi: 10.1093/nar/gky448
Liu, W. et al. IBS: An illustrator for the presentation and visualization of biological sequences. Bioinformatics 31, 3359–3361 (2015).
pubmed: 26069263
pmcid: 4595897
doi: 10.1093/bioinformatics/btv362
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
pubmed: 28263959
pmcid: 5600148
doi: 10.1038/nmeth.4197
Ren, M. et al. Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol. 155, 1367–1382 (2011).
pubmed: 21266656
pmcid: 3046592
doi: 10.1104/pp.110.169045
Nietzsche, M., Schießl, I. & Börnke, F. The complex becomes more complex: protein-protein interactions of SnRK1 with DUF581 family proteins provide a framework for cell- and stimulus type-specific SnRK1 signaling in plants. Front Plant Sci. 5, 54 (2014).
pubmed: 24600465
pmcid: 3930858
doi: 10.3389/fpls.2014.00054