CsSh5.1, which controls hypocotyl elongation under high temperature conditions in cucumber, was mapped to a 57.1 kb region on chromosome 5 containing a candidate gene encoding a xyloglucan galactosyltransferase.
Hypocotyl growth is a vital process in seedling establishment. Hypocotyl elongation after germination relies more on longitudinal cell elongation than cell division. Cell elongation is largely determined by the extensibility of the cell wall. Here, we identified a spontaneous mutant in cucumber (Cucumis sativus L.), sh5.1, which exhibits a temperature-insensitive short hypocotyl phenotype. Genetic analysis showed that the phenotype of sh5.1 was controlled by a recessive nuclear gene. CsSh5.1 was mapped to a 57.1 kb interval on chromosome 5, containing eight predicted genes. Sequencing analysis revealed that the Csa5G171710 is the candidate gene of CsSh5.1, which was further confirmed via co-segregation analysis and genomic DNA sequencing in natural cucumber variations. The result indicated that hypocotyl elongation might be controlled by this gene. CsSh5.1 encodes a xyloglucan galactosyltransferase that specifically adds galactose to xyloglucan and forms galactosylated xyloglucans, which determine the strength and extensibility of the cell walls. CsSh5.1 expression in wild-type (WT) hypocotyl was significantly higher than that in sh5.1 hypocotyl under high temperature, suggesting its important role in hypocotyl cell elongation under high temperature. The identification of CsSh5.1 is helpful for elucidating the function of xyloglucan galactosyltransferase in cell wall expansion and understanding the mechanism of hypocotyl elongation in cucumber.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLOS GENET 2:e106
Bo K, Wang H, Pan Y, Behera TK, Pandey S, Wen C, Wang Y, Simon PW, Li Y, Chen J, Weng Y (2016) SHORT HYPOCOTYL 1 Encodes a SMARCA3-like Chromatin Remodeling Factor Regulating Elongation. Plant Physiol 172:501–2016
Boron AK, Vissenberg K (2014) The Arabidopsis thaliana hypocotyl, a model to identify and study control mechanisms of cellular expansion. Plant Cell Rep 33:697–706
Box MS, Huang BE, Domijan M, Jaeger KE, Khattak AK, Yoo SJ, Sedivy EL, Jones DM, Hearn TJ, Webb AAR, Grant A, Locke JCW, Wigge PA (2015) ELF3 controls thermoresponsive growth in Arabidopsis. Curr Biol 25:194–199
Cavagnaro PF, Senalik DA, Yang L, Simon PW, Harkins TT, Kodira CD, Huang S, Weng Y (2010) Genome-wide characterization of simple sequence repeats in cucumber (Cucumis sativus L.). Bmc Genomics 11:569
Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326
Crawford AJ, McLachlan DH, Hetherington AM, Franklin KA (2012) High temperature exposure increases plant cooling capacity. Curr Biol 22:R396–R397
Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, Ye S, Yu P, Breen G, Cohen JD, Wigge PA, Gray WM (2011) Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci 108:20231–20235
Gangappa SN, Kumar SV (2017) DET1 and HY5 control PIF4-mediated thermosensory elongation growth through distinct mechanisms. Cell Rep 18:344–351
Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Hofte H (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114:295–305
Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M (1998) High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci 95:7197–7202
Harholt J, Suttangkakul A, Vibe Scheller H (2010) Biosynthesis of Pectin. Plant Physiol 153:384–395
Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P, Ren Y, Zhu H, Li J, Lin K, Jin W, Fei Z, Li G, Staub J, Kilian A, van der Vossen EAG, Wu Y, Guo J, He J, Jia Z, Ren Y, Tian G, Lu Y, Ruan J, Qian W, Wang M, Huang Q, Li B, Xuan Z, Cao J, Asan WuZ, Zhang J, Cai Q, Bai Y, Zhao B, Han Y, Li Y, Li X, Wang S, Shi Q, Liu S, Cho WK, Kim J, Xu Y, Heller-Uszynska K, Miao H, Cheng Z, Zhang S, Wu J, Yang Y, Kang H, Li M, Liang H, Ren X, Shi Z, Wen M, Jian M, Yang H, Zhang G, Yang Z, Chen R, Liu S, Li J, Ma L, Liu H, Zhou Y, Zhao J, Fang X, Li G, Fang L, Li Y, Liu D, Zheng H, Zhang Y, Qin N, Li Z, Yang G, Yang S, Bolund L, Kristiansen K, Zheng H, Li S, Zhang X, Yang H, Wang J, Sun R, Zhang B, Jiang S, Wang J, Du Y, Li S (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281
Hwang G, Zhu J, Lee YK, Kim S, Nguyen TT, Kim J, Oh E (2017) PIF4 promotes expression of LNG1 and LNG2 to induce thermomorphogenic growth in Arabidopsis. Front Plant Sci 8:1320
Jensen JK, Schultink A, Keegstra K, Wilkerson CG, Pauly M (2012) RNA-seq analysis of developing nasturtium seeds (Tropaeolum majus): identification and characterization of an additional galactosyltransferase involved in xyloglucan biosynthesis. Mol Plant 5:984–992
Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1[->]4)-[beta]-D-galactan. Plant Physiol 113:1405–1412
Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JC, Schafer E, Jaeger KE, Wigge PA (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354:886–889
Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, Franklin KA (2009) High temperature-mediated adaptations in plant architecture require the b HLH transcription factor PIF4. Curr Biol 19:408–413
Kong Y, Peña MJ, Renna L, Avci U, Pattathil S, Tuomivaara ST, Li X, Reiter W, Brandizzi F, Hahn MG, Darvill AG, York WS, Neill MA O (2015) Galactose-depleted xyloglucan is dysfunctional and leads to dwarfism in Arabidopsis. Plant Physiol 167:1296–1306
Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245
Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147
Kutschera U, Niklas KJ (2013) cell division and turgor-driven stem elongation in juvenile plants: a synthesis. Plant Sci 207:45–56
Legris M, Klose C, Burgie ES, Rojas CCR, Neme M, Hiltbrunner A, Wigge PA, Schäfer E, Vierstra RD, Casal JJ (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354:897–900
Madson M, Dunand C, Li X, Verma R, Vanzin GF, Caplan J, Shoue DA, Carpita NC, Reiter W (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15:1662–1670
Martínez C, Espinosa Ruíz A, Lucas M, Bernardo García S, Franco Zorrilla JM, Prat S (2018) PIF4-induced BR synthesis is critical to diurnal and thermomorphogenic growth. EMBO J 37:e99552
McCartney L, Ormerod AP, Gidley MJ, Knox JP (2000) Temporal and spatial regulation of pectic (14)-Beta-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. Plant J 22:105–113
Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci 88:9828–9832
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8:4321–4326
Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4–ELF3–LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402
Oh E, Zhu J, Wang Z (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14:802–809
Peña MJ, Ryden P, Madson M, Smith AC, Carpita NC (2004) The galactose residues of Xyloglucan are essential to maintain mechanical strength of the primary cell walls in Arabidopsis during growth. Plant Physiol 134:443–451
Pierre J, Teulat B, Juchaux M, Mabilleau G, Demilly D, Dürr C (2014) Cellular changes during Medicago truncatula hypocotyl growth depend on temperature and genotype. Plant Sci 217–218:18–26
Powell AE, Lenhard M (2012) Control of organ size in plants. Curr Biol 22:R360–R367
Proveniers MCG, van Zanten M (2013) High temperature acclimation through PIF4 signaling. Trends Plant Sci 18:59–64
Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, van Zanten M (2016) Molecular and genetic control of plant thermomorphogenesis. Nat Plants 2(1):9
Raschke A, Ibañez C, Ullrich KK, Anwer MU, Becker S, Glöckner A, Trenner J, Denk K, Saal B, Sun X, Ni M, Davis SJ, Delker C, Quint M (2015) Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes. BMC Plant Biol 15(1):10
Raz V, Koornneef M (2001) Cell division activity during apical hook development1. Plant Physiol (Bethesda) 125:219–226
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Salamov AA (2000) Ab initio gene finding in drosophila genomic DNA. Genome Res 10:516–522
Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682
Simon P (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19:1439–1440
Sun J, Qi L, Li Y, Chu J, Li C (2012) PIF4–mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating arabidopsis hypocotyl growth. PLOS Genet 8:e1002594
Thines B, Harmon FG (2010) Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc Natl Acad Sci 107:3257–3262
Tuomivaara ST, Yaoi K, Neill O, MA, York WS, (2015) Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature. Carbohyd Res 402:56–66
Wang H, Shang Q (2020) The combined effects of light intensity, temperature, and water potential on wall deposition in regulating hypocotyl elongation of Brassica rapa. peer J 8:e9106
Wigge PA (2013) Ambient temperature signaling in plants. Curr Opin Plant Biol 16:661–666
Xu Z, Wang M, Shi D, Zhou G, Niu T, Hahn MG, Neill MA Y Kong O (2017) DGE-seq analysis of MUR3-related Arabidopsis mutants provides insight into how dysfunctional xyloglucan affects cell elongation. Plant Sci 258:156–169
Zhang W, Pan J, He H, Zhang C, Li Z, Zhao J, Yuan X, Zhu L, Huang S, Cai R (2012) Construction of a high density integrated genetic map for cucumber (Cucumis sativus L.). Theor Appl Genet 124:249–259
We thank Lihuang Zhu (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) for affording technical support for the experiment. This study was supported by the Project of Science and Technology Commission of Shanghai Municipality (18391900300), the National Natural Science Foundation of China (no. 31672173), the National Natural Science Foundation of China (31972425), and. the Agri-X Interdisciplinary Fund of Shanghai Jiao Tong Univerity (Agri-X2017011).
Conflict of interest
The authors declare that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by Sanwen Huang.
About this article
Cite this article
Zhang, K., Pan, J., Chen, Y. et al. Mapping and identification of CsSh5.1, a gene encoding a xyloglucan galactosyltransferase required for hypocotyl elongation in cucumber (Cucumis sativus L.). Theor Appl Genet 134, 979–991 (2021). https://doi.org/10.1007/s00122-020-03754-2