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The peach (Prunus persica [L.] Batsch) homeobox gene KNOPE3, which encodes a class 2 knotted-like transcription factor, is regulated during leaf development and triggered by sugars

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Abstract

Class 1 KNOTTED1-like transcription factors (KNOX) are known to regulate plant development, whereas information on class 2 KNOX has been limited. The peach KNOPE3 gene was cloned, belonged to a family of few class 2 members and was located at 66 cM in the Prunus spp. G1 linkage-group. The mRNA localization was diversified in leaf, stem, flower and drupe, but recurred in all organ sieves, suggesting a role in sap nutrient transport. During leaf development, the mRNA earliest localized to primordia sieves and subsequently to mesophyll cells of growing leaves. Consistently, its abundance augmented with leaf expansion. The transcription was monitored in leaves responding to darkening, supply and transport block of sugars. It peaked at 4 h after darkness and dropped under prolonged obscurity, showing a similar kinetic to that of sucrose content variation. Feeding leaflets via the transpiration stream caused KNOPE3 up-regulation at 3 h after fructose, glucose and sucrose absorption and at 12 h after sorbitol. In girdling experiments, leaf KNOPE3 was triggered from 6 h onwards along with sucrose and sorbitol raise. Both the phloem-associated expression and sugar-specific gene modulation suggest that KNOPE3 may play a role in sugar translocation during the development of agro-relevant organs such as drupe.

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References

  • An YQ, McDowell JM, Huang S, McKinney EC, Chambliss S, Meagher RB (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J 10:107–121

    Article  PubMed  CAS  Google Scholar 

  • Bassett C (2007) Regulation of gene expression in plants. The role of transcript structure and processing. Springer, Heidelberg

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cañas L, Busscher M, Angenent G, Beltran J, van Tunen A (1994) Nuclear localization of the petunia MADS box protein FBP1. Plant J 6:597–604

    Article  Google Scholar 

  • Chandler J, Wolfgang W (2004) KNAT3 and KNAT4: two KNOX genes control multiple aspects of plant development and are active in the shoot apical meristem. 15th International conference on Arabidopsis research. Berlin

  • Church G, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Article  PubMed  CAS  Google Scholar 

  • Cole M, Nolte C, Werr W (2006) Nuclear import of the transcription factor SHOOT MERISTEMLESS depends on heterodimerization with BLH proteins expressed in discrete sub-domains of the shoot apical meristem of Arabidopsis thaliana. Nucleic Acids Res 34:1281–1292

    Article  PubMed  CAS  Google Scholar 

  • Di Giacomo E, Sestili F, Iannelli MA, Testone G, Mariotti D, Frugis G (2008) Characterization of KNOX genes in Medicago truncatula. Plant Mol Biol 67:135–150

    Article  PubMed  CAS  Google Scholar 

  • Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldere F, Cosson P, Howad W, Arus P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 101:9891–9896

    Article  PubMed  CAS  Google Scholar 

  • Giannino D, Frugis G, Ticconi C, Florio S, Mele G, Santini L, Cozza R, Bitonti MB, Innocenti A, Mariotti D (2000) Isolation and molecular characterisation of the gene encoding the cytoplasmic ribosomal protein S28 in Prunus persica [L.] Batsch. Mol Gen Genet 263:201–212

    Article  PubMed  CAS  Google Scholar 

  • Giannino D, Condello E, Bruno L, Testone G, Tartarini A, Cozza R, Innocenti AM, Bitonti MB, Mariotti D (2004) The gene geranylgeranyl reductase of peach (Prunus persica [L.] Batsch) is regulated during leaf development and responds differentially to distinct stress factors. J Exp Bot 55:2063–2073

    Article  PubMed  CAS  Google Scholar 

  • Graber JH, Cantor CR, Mohr SC, Smith TF (1999) In silico detection of control signals: mRNA 3′-end-processing sequences in diverse species. Proc Natl Acad Sci USA 96:14055–14060

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Guo M, Thomas J, Collins G, Timmermans MC (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20:48–58

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hake S, Smith HM, Holtan H, Magnani E, Mele G, Ramirez J (2004) The role of knox genes in plant development. Annu Rev Cell Dev Biol 20:125–151

    Article  PubMed  CAS  Google Scholar 

  • Harrison J, Moller M, Langdale J, Cronk Q, Hudson A (2005) The role of KNOX genes in the evolution of morphological novelty in Streptocarpus. Plant Cell 17:430–443

    Article  PubMed  CAS  Google Scholar 

  • Hay A, Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38:942–947

    Article  PubMed  CAS  Google Scholar 

  • Hay A, Craft J, Tsiantis M (2004) Plant hormones and homeoboxes: bridging the gap? Bioessays 26:395–404

    Article  PubMed  CAS  Google Scholar 

  • Hofer J, Gourlay C, Michael A, Ellis TH (2001) Expression of a class 1 knotted1-like homeobox gene is down-regulated in pea compound leaf primordia. Plant Mol Biol 45:387–398

    Article  PubMed  CAS  Google Scholar 

  • Janssen BJ, Williams A, Chen JJ, Mathern J, Hake S, Sinha N (1998) Isolation and characterization of two knotted-like homeobox genes from tomato. Plant Mol Biol 36:417–425

    Article  PubMed  CAS  Google Scholar 

  • Joobeur T, Viruel M, de Vicente M, Jàuregui B, Ballester J, Dettori M, Verde I, Truco M, Messeguer R, Batlle I, Quarta R, Dirlewanger E, Arùs P (1998) Construction of a saturated linkage map for Prunus using an almond peach F2 progeny. Theor Appl Genet 97:1034–1041

    Article  CAS  Google Scholar 

  • Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S (1994) Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6:1877–1887

    Article  PubMed  CAS  Google Scholar 

  • Kim JY, Rim Y, Wang J, Jackson D (2005) A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev 19:788–793

    Article  PubMed  CAS  Google Scholar 

  • Kimura S, Koenig D, Kang J, Yoong FY, Sinha N (2008) Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr Biol 18:672–677

    Article  PubMed  CAS  Google Scholar 

  • Kingston RE, Chomczynski P, Sacchi N (2001) Guanidine methods for total RNA preparation. Curr Protoc Mol Biol Chap 4, Unit 4.2

  • Kitamura-Abe S, Itoh H, Washio T, Tsutsumi A, Tomita M (2004) Characterization of the splice sites in GT-AG and GC-AG introns in higher eukaryotes using full-length cDNAs. J Bioinform Comput Biol 2:309–331

    Article  PubMed  CAS  Google Scholar 

  • Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Krapp A, Quick W, Stitt M (1991) Ribulose-1, 5-bisphosphate carboxylase-oxygenase, other Calvin-cycle enzymes, and chlorophyll decrease when glucose is supplied to mature spinach leaves via the transpiration stream. Planta 186:58–69

    Article  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Li H, Xu L, Wang H, Yuan Z, Cao X, Yang Z, Zhang D, Xu Y, Huang H (2005) The Putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and MicroRNA165/166 in Arabidopsis leaf development. Plant Cell 17:2157–2171

    Article  PubMed  CAS  Google Scholar 

  • Lin JF, Wu SH (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628

    Article  PubMed  CAS  Google Scholar 

  • Lincoln S, Daly M, Lander E (1992) Mapping genes controlling quantitative traits with MAPMAKER/QTL, 2nd edn. Whitehead Institute Technical Report, Cambridge

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lo Bianco R, Rieger M, Sung SJ (1999) Carbohydrate metabolism of vegetative and reproductive sinks in the late-maturing peach cultivar ‘Encore’. Tree Physiol 19:103–109

    PubMed  CAS  Google Scholar 

  • Magnani E, Hake S (2008) KNOX lost the OX: the Arabidopsis KNATM gene defines a novel class of KNOX transcriptional regulators missing the homeodomain. Plant Cell 20:875–887

    Article  PubMed  CAS  Google Scholar 

  • Maurel K, Leite GB, Bonhomme M, Guilliot A, Rageau R, Petel G, Sakr S (2004) Trophic control of bud break in peach (Prunus persica) trees: a possible role of hexoses. Tree Physiol 24:579–588

    PubMed  CAS  Google Scholar 

  • Merlo L, Passera C (1991) Changes in carbohydrates and enzyme levels during development of leaves of Prunus persica: a sorbitol synthesizing species. Physiol Plant 83:621–626

    Article  CAS  Google Scholar 

  • Moing A, Carbonne R, Zipperlin B, Svanella L, Gaudillere J (1997) Phloem loading in peach: sympiastic or apoplastic? Physiol Plant 101:489–496

    Article  CAS  Google Scholar 

  • Morandi B, Rieger M, Grappadelli LC (2007) Vascular flows and transpiration affect peach (Prunus persica Batsch.) fruit daily growth. J Exp Bot 58:3941–3947

    Article  PubMed  CAS  Google Scholar 

  • Morere-Le Paven MC, Anzala F, Recton A, Limami AM (2007) Differential transcription initiation and alternative RNA splicing of Knox7, a class 2 homeobox gene of maize. Gene 401:71–79

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Pagnussat GC, Yu HJ, Sundaresan 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

    Article  PubMed  CAS  Google Scholar 

  • Porra R, Thompson W, Kriedemann P (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophylls standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150

    Article  PubMed  CAS  Google Scholar 

  • Reiser L, Sanchez-Baracaldo P, Hake S (2000) Knots in the family tree: evolutionary relationships and functions of knox homeobox genes. Plant Mol Biol 42:151–166

    Article  PubMed  CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  PubMed  CAS  Google Scholar 

  • Sanchez Perez R, Howad W, Dicenta F, Arus P, Martinez-Gomez P (2007) Mapping major genes and quantitative trait loci controlling agronomic traits in almond. Plant Breed 126:310–318

    Article  CAS  Google Scholar 

  • Schutze K, Harter K, Chaban C (2008) Post-translational regulation of plant bZIP factors. Trends Plant Sci 13:247–255

    Article  PubMed  Google Scholar 

  • Scofield S, Murray JA (2006) KNOX gene function in plant stem cell niches. Plant Mol Biol 60:929–946

    Article  PubMed  CAS  Google Scholar 

  • Sentoku N, Tamaoki M, Nishimura A, Matsuoka M (1998) The homeobox gene NTH23 of tobacco is expressed in the basal region of leaf primordia. Biochim Biophys Acta 1399:203–208

    PubMed  CAS  Google Scholar 

  • Serikawa KA, Martinez-Laborda A, Zambryski P (1996) Three knotted1-like homeobox genes in Arabidopsis. Plant Mol Biol 32:673–683

    Article  PubMed  CAS  Google Scholar 

  • Serikawa KA, Martinez-Laborda A, Kim HS, Zambryski PC (1997) Localization of expression of KNAT3, a class 2 knotted1-like gene. Plant J 11:853–861

    Article  PubMed  CAS  Google Scholar 

  • Singer SD, Ashton NW (2007) Revelation of ancestral roles of KNOX genes by a functional analysis of Physcomitrella homologues. Plant Cell Rep 26:2039–2054

    Article  PubMed  CAS  Google Scholar 

  • Smith AM, Zeeman SC, Thorneycroft D, Smith SM (2003) Starch mobilization in leaves. J Exp Bot 54:577–583

    Article  PubMed  CAS  Google Scholar 

  • Soucek P, Klima P, Rekova A, Brzobohaty B (2007) Involvement of hormones and KNOXI genes in early Arabidopsis seedling development. J Exp Bot 58:3797–3810

    Article  PubMed  CAS  Google Scholar 

  • Tamaoki M, Tsugawa H, Minami E, Kayano T, Yamamoto N, Kano-Murakami Y, Matsuoka M (1995) Alternative RNA products from a rice homeobox gene. Plant J 7:927–938

    Article  PubMed  CAS  Google Scholar 

  • Testone G, Bruno L, Condello E, Chiappetta A, Bruno A, Mele G, Tartarini A, Spano L, Innocenti AM, Mariotti D, Bitonti MB, Giannino D (2008) Peach [Prunus persica (L.) Batsch] KNOPE1, a class 1 KNOX orthologue to Arabidopsis BREVIPEDICELLUS/KNAT1, is misexpressed during hyperplasia of leaf curl disease. J Exp Bot 59:389–402

    Article  PubMed  CAS  Google Scholar 

  • Thum KE, Shin MJ, Gutierrez RA, Mukherjee I, Katari MS, Nero D, Shasha D, Coruzzi GM (2008) An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis. BMC Syst Biol 2:31

    Article  PubMed  Google Scholar 

  • Truernit E, Siemering KR, Hodge S, Grbic V, Haseloff J (2006) A map of KNAT gene expression in the Arabidopsis root. Plant Mol Biol 60:1–20

    Article  PubMed  CAS  Google Scholar 

  • Vemmos S, Goldwin G (1994) The photosynthetic activity of Cox’s Orange Pippin apple flowers in relation to fruit setting. Ann Botany 73:385–391

    Article  Google Scholar 

  • Watillon B, Kettmann R, Boxus P, Burny A (1993) Developmental and circadian pattern of rubisco activase mRNA accumulation in apple plants. Plant Mol Biol 23:501–509

    Article  PubMed  CAS  Google Scholar 

  • Watillon B, Kettmann R, Boxus P, Burny A (1997) Knotted1-like homeobox genes are expressed during apple tree (Malus domestica [L.] Borkh) growth and development. Plant Mol Biol 33:757–763

    Article  PubMed  CAS  Google Scholar 

  • Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886

    Article  PubMed  CAS  Google Scholar 

  • Yamaki S (1980) Properties and function of sorbitol-6-phosphate dehydrogenase, sorbitol dehydrogenase and sorbitol oxidase in fruit and cotyledon of apple Malus pumila Mill. var.domestica Schneid. J Japan Soc Hort Sci 49:429–434

    Article  CAS  Google Scholar 

  • Yoshii A, Shimizu T, Yoshida A, Hamada K, Sakurai K, Yamaji Y, Suzuki M, Namba S, Hibi T (2008) NTH201, a novel class II KNOTTED1-like protein, facilitates the cell-to-cell movement of Tobacco mosaic virus in tobacco. Mol Plant Microbe Interact 21:586–596

    Article  PubMed  CAS  Google Scholar 

  • Zanchin A, Bonghi C, Casadoro G, Ramina A, Rascio N (1994) Cell enlargement and cell separation during peach fruit development. Int J Plant Sci 155:49–56

    Article  Google Scholar 

  • Zhong R, Richardson EA, Ye ZH (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19:2776–2792

    Article  PubMed  CAS  Google Scholar 

  • Zhou R, Cheng L, Dandekar AM (2006) Down-regulation of sorbitol dehydrogenase and up-regulation of sucrose synthase in shoot tips of the transgenic apple trees with decreased sorbitol synthesis. J Exp Bot 57:3647–3657

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Chiara Nicolodi and Mauro Santini (IBBA-CNR) for technical support, Dr. Samuel Forrest (Clemson University, SC, US) for criticism and English revision. Financial sustains derived from the UNICAL (E.C. was awarded by a PhD scholarship), the project “Eumorfo” of CRA-MIPAF and the CNR Agro-food Department (Director Alcide Bertani). This work is dedicated to the memory of our guide Domenico Mariotti (1948–2008).

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Correspondence to Donato Giannino.

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Communicated by H. Ronne.

G. Testone and E. Condello have been equally contributed to the work.

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438_2009_445_MOESM1_ESM.doc

Exons are typed in black, introns in italics. Intron consensuses are underlined. Sequences of primers are capitalised; primer names and orientation are shaded in red. Hinc II sites are double-underlined. (DOC 36 kb)

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Testone, G., Condello, E., Verde, I. et al. The peach (Prunus persica [L.] Batsch) homeobox gene KNOPE3, which encodes a class 2 knotted-like transcription factor, is regulated during leaf development and triggered by sugars. Mol Genet Genomics 282, 47–64 (2009). https://doi.org/10.1007/s00438-009-0445-7

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