Abstract
Key message
AtHSPR forms a complex with KNAT5 and OFP1 to regulate primary root growth through GA-mediated root meristem activity. KNAT5–OFP1 functions as a negative regulator of AtHSPR in response to GA.
Abstract
Plant root growth is modulated by gibberellic acid (GA) signaling and depends on root meristem maintenance. ARABIDOPSIS THALIANA HEAT SHOCK PROTEIN-RELATED (AtHSPR) is a vital regulator of flowering time and salt stress tolerance. However, little is known about the role of AtHSPR in the regulation of primary root growth. Here, we report that athspr mutant exhibits a shorter primary root compared to wild type and that AtHSPR interacts with KNOTTED1-LIKE HOMEOBOX GENE 5 (KNAT5) and OVATE FAMILY PROTEIN 1 (OFP1). Genetic analysis showed that overexpression of KNAT5 or OFP1 caused a defect in primary root growth similar to that of the athspr mutant, but knockout of KNAT5 or OFP1 rescued the short root phenotype in the athspr mutant by altering root meristem activity. Further investigation revealed that KNAT5 interacts with OFP1 and that AtHSPR weakens the inhibition of GIBBERELLIN 20-OXIDASE 1 (GA20ox1) expression by the KNAT5–OFP1 complex. Moreover, root meristem cell proliferation and root elongation in 35S::KNAT5athspr and 35S::OFP1athspr seedlings were hypersensitive to GA3 treatment compared to the athspr mutant. Together, our results demonstrate that the AtHSPR–KNAT5–OFP1 module regulates root growth and development by impacting the expression of GA biosynthetic gene GA20ox1, which could be a way for plants to achieve plasticity in response to the environment.
Similar content being viewed by others
Data availability
All data supporting the findings of this study are available within the paper and within its supplementary data published online. Further inquiries can be directed to the corresponding author.
Abbreviations
- AtHSPR:
-
ARABIDOPSIS THALIANA HEAT SHOCK PROTEIN-RELATED
- GA:
-
Gibberellic acid
- GA20OX:
-
GA 20-OXIDASE
- KNAT5:
-
KNOTTED1-LIKE HOMEOBOX GENE 5
- MZ:
-
Meristematic zone
- OFP1:
-
OVATE FAMILY PROTEIN 1
- PAC:
-
Paclobutrazol
- WT:
-
Wild type
References
Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GTS, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19:1188–1193. https://doi.org/10.1016/j.cub.2009.05.059
Beemster GTS, Baskin TI (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116:1515–1526. https://doi.org/10.1104/pp.116.4.1515
Belda-Palazon B, Costa M, Beeckman T, Rolland F, Baena-Gonzalez E (2022) ABA represses TOR and root meristem activity through nuclear exit of the SnRK1 kinase. Proc Natl Acad Sci USA 119:e2204862119. https://doi.org/10.1073/pnas.2204862119
Bellaoui M, Pidkowich MS, Samach A, Kushalappa K, Kohalmi SE, Modrusan Z, Crosby WL, Haughn GW (2001) The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell 13:2455–2470. https://doi.org/10.1105/tpc.010161
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44. https://doi.org/10.1038/nature03184
Bos JIB, Armstrong MR, Gilroy EM, Boevink PC, Hein I, Taylor RM, Zhendong T, Engelhardt S, Vetukuri RR, Harrower B, Dixelius C, Bryan G, Sadanandom A, Whisson SC, Kamoun S, Birch PRJ (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc Natl Acad Sci USA 107:9909–9914. https://doi.org/10.1073/pnas.2019643117
Brown DM, Zeef LAH, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295. https://doi.org/10.1105/tpc.105.031542
Burglin TR (1997) Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res 25:4173–4180. https://doi.org/10.1093/nar/25.21.4173
Cao J, Liang Y, Yan T, Wang X, Zhou H, Chen C, Zhang Y, Zhang B, Zhang S, Liao J, Cheng S, Chu J, Huang X, Xu D, Li J, Deng XW, Lin F (2022) The photomorphogenic repressors BBX28 and BBX29 integrate light and brassinosteroid signaling to inhibit seedling development in Arabidopsis. Plant Cell 34:2266–2285. https://doi.org/10.1093/plcell/koac092
Chen H, Banerjee AK, Hannapel DJ (2004) The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J 38:276–284. https://doi.org/10.1111/j.1365-313X.2004.02048.x
Chen YY, Wang ZP, Ni HW, Xu Y, Chen QJ, Jiang LJ (2017) CRISPR/Cas9-mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis. Sci China Life Sci 60:520–523. https://doi.org/10.1007/s11427-017-9021-5
de Dorlodot S, Forster B, Pages L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12:474–481. https://doi.org/10.1016/j.tplants.2007.08.012
Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384. https://doi.org/10.1126/science.1164147
Du J, Mansfield SD, Groover AT (2009) The Populus homeobox gene ARBORKNOX2 regulates cell differentiation during secondary growth. Plant J 60:1000–1014. https://doi.org/10.1111/j.1365-313X.2009.04017.x
Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song KM, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629. https://doi.org/10.1111/j.1365-313X.2005.02617.x
Furumizu C, Alvarez JP, Sakakibara K, Bowman JL (2015) Antagonistic roles for KNOX1 and KNOX2 genes in patterning the land plant body plan following an ancient gene duplication. PLoS Genet 11:e1004980. https://doi.org/10.1371/journal.pgen.1004980
Groover AT, Mansfield SD, DiFazio SP, Dupper G, Fontana JR, Millar R, Wang Y (2006) The Populus homeobox gene ARBORKNOX1 reveals overlapping mechanisms regulating the shoot apical meristem and the vascular cambium. Plant Mol Biol 61:917–932. https://doi.org/10.1007/s11103-006-0059-y
Hackbusch J, Richter K, Muller J, Salamini F, Uhrig JF (2005) A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc Natl Acad Sci USA 102:4908–4912. https://doi.org/10.1073/pnas.0501181102
Hashem AM, Moore S, Chen S, Hu C, Zhao Q, Elesawi IE, Feng Y, Topping JF, Liu J, Lindsey K, Chen C (2021) Putrescine depletion affects Arabidopsis root meristem size by modulating auxin and cytokinin signaling and ROS accumulation. Int J Mol Sci. https://doi.org/10.3390/ijms22084094
Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12:1557–1565. https://doi.org/10.1016/S0960-9822(02)01125-9
Israelsson M, Mellerowicz E, Chono M, Gullberg J, Moritz T (2004) Cloning and overproduction of gibberellin 3-oxidase in hybrid aspen trees. Effects of gibberellin homeostasis and development. Plant Physiol 135:221–230. https://doi.org/10.1104/pp.104.038935
Jathar V, Saini K, Chauhan A, Rani R, Ichihashi Y, Ranjan A (2022) Spatial control of cell division by GA-OsGRF7/8 module in a leaf explaining the leaf length variation between cultivated and wild rice. New Phytol 234:867–883. https://doi.org/10.1111/nph.18029
Jiang K, Feldman LJ (2005) Regulation of root apical meristem development. Annu Rev Cell Dev Biol 21:485–509. https://doi.org/10.1146/annurev.cellbio.21.122303.114753
Kanrar S, Onguka O, Smith HMS (2006) Arabidopsis inflorescence architecture requires the activities of KNOX-BELL homeodomain heterodimers. Planta 224:1163–1173. https://doi.org/10.1007/s00425-006-0298-9
Katayama Y, Gottesman S, Pumphrey J, Rudikoff S, Clark WP, Maurizi MR (1988) The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J Biol Chem 263:15226–15236
Khosla A, Nelson DC (2016) Strigolactones, super hormones in the fight against Striga. Curr Opin Plant Biol 33:57–63. https://doi.org/10.1016/j.pbi.2016.06.001
Lantzouni O, Alkofer A, Falter-Braun P, Schwechheimer C (2020) GROWTH-REGULATING FACTORS interact with DELLAs and regulate growth in cold stress. Plant Cell 32:1018–1034. https://doi.org/10.1105/tpc.19.00784
Li EY, Wang SC, Liu YY, Chen JG, Douglas CJ (2011) OVATE FAMILY PROTEIN4 (OFP4) interaction with KNAT7 regulates secondary cell wall formation in Arabidopsis thaliana. Plant J 67:328–341. https://doi.org/10.1111/j.1365-313X.2011.04595.x
Li JT, Zhao Y, Chu HW, Wang LK, Fu YR, Liu P, Upadhyaya N, Chen CL, Mou TM, Feng YQ, Kumar P, Xu J (2015) SHOEBOX modulates root meristem size in rice through dose-dependent effects of gibberellins on cell elongation and proliferation. PLoS Genet 11:e1005464. https://doi.org/10.1371/journal.pgen.1005464
Li J, Yang Y, Chai M, Ren M, Yuan J, Yang W, Dong Y, Liu B, Jian Q, Wang S, Peng B, Yuan H, Fan H (2020) Gibberellins modulate local auxin biosynthesis and polar auxin transport by negatively affecting flavonoid biosynthesis in the root tips of rice. Plant Sci 298:110545. https://doi.org/10.1016/j.plantsci.2020.110545
Liebsch D, Sunaryo W, Holmlund M, Norberg M, Zhang J, Hall HC, Helizon H, Jin X, Helariutta Y, Nilsson O, Polle A, Fischer U (2014) Class I KNOX transcription factors promote differentiation of cambial derivatives into xylem fibers in the Arabidopsis hypocotyl. Development 141:4311–4319. https://doi.org/10.1242/dev.111369
Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6:1859–1876. https://doi.org/10.1105/tpc.6.12.1859
Lopez-Cristoffanini C, Serrat X, Jauregui O, Nogues S, Lopez-Carbonell M (2019) Phytohormone profiling method for rice: effects of GA20ox mutation on the gibberellin content of japonica rice varieties. Front Plant Sci 10:733. https://doi.org/10.3389/fpls.2019.00733
Lv BS, Tian HY, Zhang F, Liu JJ, Lu SC, Bai MY, Li CY, Ding ZJ (2018) Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. PLoS Genet 14:e1007144. https://doi.org/10.1371/journal.pgen.1007144
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049. https://doi.org/10.1104/pp.111.175414
Lyu J, Aiwaili P, Gu ZY, Xu YJ, Zhang YH, Wang ZL, Huang HF, Zeng RH, Ma C, Gao JP, Zhao X, Hong B (2022) Chrysanthemum MAF2 regulates flowering by repressing gibberellin biosynthesis in response to low temperature. Plant J 112:1159–1175. https://doi.org/10.1111/tpj.16002
Ma Q, Wang N, Hao P, Sun H, Wang C, Ma L, Wang H, Zhang X, Wei H, Yu S (2019) Genome-wide identification and characterization of TALE superfamily genes in cotton reveals their functions in regulating secondary cell wall biosynthesis. BMC Plant Biol 19:432. https://doi.org/10.1186/s12870-019-2026-1
Mitsuda N, Ohme-Takagi M (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol 50:1232–1248. https://doi.org/10.1093/pcp/pcp075
Motte H, Vanneste S, Beeckman T (2019) Molecular and environmental regulation of root development. Annu Rev Plant Biol 70:465–488. https://doi.org/10.1146/annurev-arplant-050718-100423
Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 20:1138–1143. https://doi.org/10.1016/j.cub.2010.05.035
Muller J, Wang Y, Franzen R, Santi L, Salamini F, Rohde W (2001) In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function. Plant J 27:13–23. https://doi.org/10.1046/j.1365-313x.2001.01064.x
Nookaraju A, Pandey SK, Ahlawat YK, Joshi CP (2022) Understanding the modus operandi of Class II KNOX transcription factors in secondary cell wall biosynthesis. Plants (basel). https://doi.org/10.3390/plants11040493
Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80. https://doi.org/10.1105/tpc.010476
Pagnussat GC, Yu HJ, Sundaresana V (2007) Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. Plant Cell 19:3578–3592. https://doi.org/10.1105/tpc.107.054890
Park EJ, Kim HT, Choi YI, Lee C, Nguyen VP, Jeon HW, Cho JS, Funada R, Pharis RP, Kurepin LV, Ko JH (2015) Overexpression of gibberellin 20-oxidase1 from Pinus densiflora results in enhanced wood formation with gelatinous fiber development in a transgenic hybrid poplar. Tree Physiol 35:1264–1277. https://doi.org/10.1093/treephys/tpv099
Pautot W, Dockx J, Hamant O, Kronenberger J, Grandjean O, Jublot D, Traas J (2001) KNAT2: evidence for a link between knotted-like genes and carpel development. Plant Cell 13:1719–1734
Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical meristem. Curr Opin Plant Biol 15:17–23. https://doi.org/10.1016/j.pbi.2011.10.006
Plackett AR, Powers SJ, Fernandez-Garcia N, Urbanova T, Takebayashi Y, Seo M, Jikumaru Y, Benlloch R, Nilsson O, Ruiz-Rivero O, Phillips AL, Wilson ZA, Thomas SG, Hedden P (2012) Analysis of the developmental roles of the Arabidopsis gibberellin 20-oxidases demonstrates that GA20ox1, -2, and -3 are the dominant paralogs. Plant Cell 24:941–960. https://doi.org/10.1105/tpc.111.095109
Qin H, Pandey BK, Li YX, Huang GQ, Wang J, Quan RD, Zhou JH, Zhou Y, Miao YC, Zhang DB, Bennett MJ, Huang RF (2022) Orchestration of ethylene and gibberellin signals determines primary root elongation in rice. Plant Cell 34:1273–1288. https://doi.org/10.1093/plcell/koac008
Rieu I, Ruiz-Rivero O, Fernandez-Garcia N, Griffiths J, Powers SJ, Gong F, Linhartova T, Eriksson S, Nilsson O, Thomas SG, Phillips AL, Hedden P (2008) The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. Plant J 53:488–504. https://doi.org/10.1111/j.1365-313X.2007.03356.x
Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590. https://doi.org/10.1101/gad.867901
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
Shekhar V, Stckle D, Thellmann M, Vermeer JEM (2019) The role of plant root systems in evolutionary adaptation. Curr Top Dev Biol 131:55–80. https://doi.org/10.1016/bs.ctdb.2018.11.011
Shi S, Li D, Li S, Wang Y, Tang X, Liu Y, Ge H, Chen H (2023) Comparative transcriptomic analysis of early fruit development in eggplant (Solanum melongena L.) and functional characterization of SmOVATE5. Plant Cell Rep 42:321–336. https://doi.org/10.1007/s00299-022-02959-7
Shimotohno A, Aki SS, Takahashi N, Umeda M (2021) Regulation of the plant cell cycle in response to hormones and the environment. Annu Rev Plant Biol 72:273–296. https://doi.org/10.1146/annurev-arplant-080720-103739
Song X, Zhao Y, Wang J, Lu MZ (2021) The transcription factor KNAT2/6b mediates changes in plant architecture in response to drought via down-regulating GA20ox1 in Populus alba × P. glandulosa. J Exp Bot 72:5625–5637. https://doi.org/10.1093/jxb/erab201
Spielmeyer W, Ellis M, Robertson M, Ali S, Lenton JR, Chandler PM (2004) Isolation of gibberellin and metabolic pathway genes from barley and comparative mapping in barley, wheat and rice. Theor Appl Genet 109:847–855. https://doi.org/10.1007/s00122-004-1689-6
Stemmer M, Thumberger T, Keyer MD, Wittbrodt J, Mateo JL (2017) CCTop: an intuitive, flexible and reliable CRISPR/Cas9 target prediction tool. PLoS One 10:e0124633. https://doi.org/10.1371/journal.pone.0176619
Tan FQ, Wang W, Li J, Lu Y, Zhu B, Hu F, Li Q, Zhao Y, Zhou DX (2022) A coiled-coil protein associates Polycomb Repressive Complex 2 with KNOX/BELL transcription factors to maintain silencing of cell differentiation-promoting genes in the shoot apex. Plant Cell 34:2969–2988. https://doi.org/10.1093/plcell/koac133
Truernit E, Haseloff J (2007) A role for KNAT class II genes in root development. Plant Signal Behav 2:10–12. https://doi.org/10.4161/psb.2.1.3604
Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GT, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628. https://doi.org/10.1038/ncb1726
Ubeda-Tomas S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19:1194–1199. https://doi.org/10.1016/j.cub.2009.06.023
van der Knaap E, Kim JH, Kende H (2000) A novel gibberellin-induced gene from rice and its potential regulatory role in stem growth. Plant Physiol 122:695–704. https://doi.org/10.1104/pp.122.3.695
van der Knaap E, Chakrabarti M, Chu YH, Clevenger JP, Illa-Berenguer E, Huang Z, Keyhaninejad N, Mu Q, Sun L, Wang Y, Wu S (2014) What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape. Front Plant Sci 5:227. https://doi.org/10.3389/fpls.2014.00227
Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, Keller W, Martienssen R, Selvaraj G, Datla R (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci USA 99:4730–4735. https://doi.org/10.1073/pnas.072626099
Wallner ES, Lopez-Salmeron V, Belevich I, Poschet G, Jung I, Grunwald K, Sevilem I, Jokitalo E, Hell R, Helariutta Y, Agusti J, Lebovka I, Greb T (2017) Strigolactone- and Karrikin-independent SMXL proteins are central regulators of phloem formation. Curr Biol 27:1241–1247. https://doi.org/10.1016/j.cub.2017.03.014
Wang S, Chang Y, Guo J, Chen JG (2007) Arabidopsis Ovate Family Protein 1 is a transcriptional repressor that suppresses cell elongation. Plant J 50:858–872. https://doi.org/10.1111/j.1365-313X.2007.03096.x
Wang ZP, Xing HL, Dong L, Zhang HY, Han CY, Wang XC, Chen QJ (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol 16:144. https://doi.org/10.1186/s13059-015-0715-0
Wang SM, Yamaguchi M, Grienenberger E, Martone PT, Samuels AL, Mansfield SD (2020) The Class II KNOX genes KNAT3 and KNAT7 work cooperatively to influence deposition of secondary cell walls that provide mechanical support to Arabidopsis stems. Plant J 101:293–309. https://doi.org/10.1111/tpj.14541
Wang M, Zhang H, Zhao X, Zhou J, Qin G, Liu Y, Kou X, Zhao Z, Wu T, Zhu JK, Feng X, Li L (2023) SYNTAXIN OF PLANTS81 regulates root meristem activity and stem cell niche maintenance via ROS signaling. Plant Physiol 191:1365–1382. https://doi.org/10.1093/plphys/kiac530
Wen B, Nieuwland J, Murray JAH (2013) The Arabidopsis CDK inhibitor ICK3/KRP5 is rate limiting for primary root growth and promotes growth through cell elongation and endoreduplication. J Exp Bot 64:1135–1144. https://doi.org/10.1093/jxb/ert009
Xiang D, Meng F, Wang A, Wu Y, Wang Z, Zheng S, Mao C (2021) Root-secreted peptide OsPEP1 regulates primary root elongation in rice. Plant J 107:480–492. https://doi.org/10.1111/tpj.15303
Xu YL, Li L, Wu KQ, Peeters AJM, Gage DA, Zeevaart JAD (1995) The GA5 locus of Arabidopsis thaliana encodes a multifunctional gibberellin 20-oxidase: molecular cloning and functional expression. Proc Natl Acad Sci USA 92:6640–6644. https://doi.org/10.1073/pnas.92.14.6640
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. https://doi.org/10.1146/annurev.arplant.59.032607.092804
Yamoune A, Cuyacot AR, Zdarska M, Hejatko J (2021) Hormonal orchestration of root apical meristem formation and maintenance in Arabidopsis. J Exp Bot 72:6768–6788. https://doi.org/10.1093/jxb/erab360
Yang T, Zhang L, Hao HY, Zhang P, Zhu HW, Cheng W, Wang YL, Wang XY, Wang CY (2015) Nuclear-localized AtHSPR links abscisic acid-dependent salt tolerance and antioxidant defense in Arabidopsis. Plant J 84:1274–1294. https://doi.org/10.1111/tpj.13080
Yang T, Sun Y, Wang YL, Zhou LN, Chen MY, Bian ZY, Lian YK, Xuan LJ, Yuan GQ, Wang XY, Wang CY (2020) AtHSPR is involved in GA- and light intensity-mediated control of flowering time and seed set in Arabidopsis. J Exp Bot 71:3543–3559. https://doi.org/10.1093/jxb/eraa128
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572. https://doi.org/10.1038/nprot.2007.199
Zhang XR, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646. https://doi.org/10.1038/nprot.2006.97
Zhang LG, Sun LL, Zhang XF, Zhang SQ, Xie DW, Liang CB, Huang WG, Fan LJ, Fang YY, Chang Y (2018) OFP1 interaction with ATH1 regulates stem growth, flowering time and flower basal boundary formation in Arabidopsis. Genes-Basel 9:399. https://doi.org/10.3390/genes9080399
Zhang YY, Yin Q, Qin WQ, Gao H, Du JG, Chen JJ, Li HL, Zhou GK, Wu H, Wu AM (2022) The Class II KNOX family members KNAT3 and KNAT7 redundantly participate in Arabidopsis seed coat mucilage biosynthesis. J Exp Bot 73:3477–3495. https://doi.org/10.1093/jxb/erac066
Zhao YQ, Song XQ, Zhou HJ, Wei KL, Jiang C, Wang JN, Cao Y, Tang F, Zhao ST, Lu MZ (2020) KNAT2/6b, a class I KNOX gene, impedes xylem differentiation by regulating NAC domain transcription factors in poplar. New Phytol 225:1531–1544. https://doi.org/10.1111/nph.16036
Zheng HY, Pan XY, Deng YX, Wu HM, Liu P, Li XX (2016) AtOPR3 specifically inhibits primary root growth in Arabidopsis under phosphate deficiency. Sci Rep-UK 6:24778. https://doi.org/10.1038/srep24778
Zhou YL, Yang Y, Niu Y, Fan TT, Qian D, Luo CX, Shi YM, Li SW, An LZ, Xiang Y (2020) The tip-localized phosphatidylserine established by Arabidopsis ALA3 is crucial for Rab GTPase-mediated vesicle trafficking and pollen tube growth. Plant Cell 32:3170–3187. https://doi.org/10.1105/tpc.19.00844
Acknowledgements
We would like to thank the Core Facility of the School of Life Sciences, Lanzhou University for kindly providing instruments and technical support.
Funding
This work was funded by the National Natural Science Foundation of China (NSFC) (Grant Nos. 31770199 and 31700215), the China Postdoctoral Science Foundation (Grant No. 2016M600824), the Foundation of the Key Laboratory of Cell Activities and Stress Adaptations, Ministry of Education of China (lzujbky-2021-kb05). The Fundamental Research Funds for the Central Universities (lzujbky-2021-43); and the Natural Science Foundation of Gansu Province, Gansu Excellent Doctoral Program (No. 23JRRA1159).
Author information
Authors and Affiliations
Contributions
CYW, GQY, and TY conceived and designed the experiments; GQY, TBY, and JMW performed the experiments; GQY, YKL, HHG, and HJW analyzed the data; GQY and YKL drafted the manuscript. All authors read and helped to polish the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
Not applicable.
Consent to participate
Yes.
Consent for publication
All authors read and approved the manuscript.
Additional information
Communicated by Zhanyuan Jon Zhang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yuan, G., Lian, Y., Wang, J. et al. AtHSPR functions in gibberellin-mediated primary root growth by interacting with KNAT5 and OFP1 in Arabidopsis. Plant Cell Rep 42, 1629–1649 (2023). https://doi.org/10.1007/s00299-023-03057-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-023-03057-y