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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

A non-cell-autonomous mechanism for the control of plant architecture and epidermal differentiation involves intercellular trafficking of BREVIPEDICELLUS protein

Yeonggil Rim A B E , Jin-Hee Jung A B E , Hyosub Chu A B , Won Kyong Cho B , Seon-Won Kim A B , Jong Chan Hong A , David Jackson C , Raju Datla D and Jae-Yean Kim A B F
+ Author Affiliations
- Author Affiliations

A Division of Applied Life Science (BK21 program), PMBBRC, Gyeongsang National University, Jinju 660-701, Republic of Korea.

B Environmental Biotechnology National Core Research Center, Gyeongsang National University, Jinju 660-701, Republic of Korea.

C Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USA.

D Plant Biotechnology Institute, National Research Council of Canada, 110 Gymnasium Place, Saskatoon, SK, Canada S7N 0W9.

E These authors contributed equally to this work.

F Corresponding author. Email: kimjy@gnu.ac.kr

Functional Plant Biology 36(3) 280-289 https://doi.org/10.1071/FP08243
Submitted: 12 September 2008  Accepted: 19 January 2009   Published: 2 March 2009

Abstract

Intercellular trafficking of maize KNOTTED1 and its homologous KNOTTED1-related homeobox (KNOX) proteins has been reported; however, little is known about the functional significance of KNOX trafficking in plant development. In this study, we showed that intercellular movement of BREVIPEDICELLUS (BP or KNAT1), the closest Arabidopsis homologue of KNOTTED1, is tissue-specific and takes place through a selective pathway. When BP was fused to a red fluorescent mCherry construct, it could move from the mesophyll to epidermal cells of leaves, although it could not move out from the cortex/endodermis of roots. Using a trichome rescue-trafficking assay, we also showed that BP fusion could confer gain-of-trafficking function to the cell-autonomous GLABROUS1 (GL1) protein. In the wild type, BP transcripts are expressed in the sub-epidermal cortical cell layers of the inflorescence stem and pedicel. However, bp mutant phenotypes include defects in epidermal cell differentiation suggesting a non-cell-autonomous function. Expression of a GFP:BP fusion under the control of a BP promoter specific to the stem cortex layers resulted in epidermal GFP fluorescence suggesting its movement from subepidermis to epidermis. Here, we provide evidence from complementation analyses using cell autonomous or non-cell-autonomous BP fusions that the intercellular trafficking of BP protein is important for plant architecture and epidermal differentiation.

Additional keywords: BREVIPEDICELLUS, KNAT1, KNOTTED1, KNOX, plasmodesmata, protein trafficking.


Acknowledgements

We thank Sunseon Kim, Dr WJ Lucas, Dr RY Tsien, Dr J Haseloff and Dr CS Pikaard for technical assistance, critical discussion, the J0571 line, the mCherry construct and the pEarleyGate construct, respectively. This work was supported by KOSEF grants to the National Research Laboratory Program (M10600000205–06J0000–20510), the WCU program (R33–2008–000–10002–0), the Environmental Biotechnology National Core Research Center (R15–2003–012–01003–0) and by the Korea Research Foundation Grant (KRF-2008–314-C00362). YR, JHJ and HC were supported by fellowships from the Brain Korea 21 Program, a program of the Korean Ministry of Education, Science and Technology.


References


Alonso-Cantabrana H, Ripoll JJ, Ochando I, Vera A, Ferrandiz C, Martinez-Laborda A (2007) Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene. Development 134, 2663–2671.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Belkhadir Y, Chory J (2006) Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science 314, 1410–1411.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ding B, Kwon MO, Hammond R, Owens R (1997) Cell-to-cell movement of potato spindle tuber viroid. The Plant Journal 12, 931–936.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. The Plant Cell 14, 547–558.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. The Plant Journal 45, 616–629.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Freeling M, Hake S (1985) Developmental genetics of mutants that specify knotted leaves in maize. Genetics 111, 617–634.
PubMed |
open url image1

Haseloff J , Hodge S (2001) Targeted gene expression in plants using GAL4. US Patent 6, 255, 558.

Hay A, Barkoulas M, Tsiantis M (2006) ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133, 3955–3961.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Current Biology 15, 1560–1565.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal 6, 3901–3907.
CAS | PubMed |
open url image1

Kim JY (2005) Regulation of short-distance transport of RNA and protein. Current Opinion in Plant Biology 8, 45–52.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kim JY, Yuan Z, Cilia M, Khalfan-Jagani Z, Jackson D (2002) Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 99, 4103–4108.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kim JY, Yuan Z, Jackson D (2003) Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130, 4351–4362.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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 & Development 19, 788–793.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S , et al . (2005a) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132, 5387–5398.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kurata T, Okada K, Wada T (2005b) Intercellular movement of transcription factors. Current Opinion in Plant Biology 8, 600–605.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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. The Plant Cell 6, 1859–1876.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lucas WJ, Bouche-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980–1983.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Mele G, Ori N, Sato Y, Hake S (2003) The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes & Development 17, 2088–2093.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307–311.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ori N, Eshed Y, Chuck G, Bowman JL, Hake S (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127, 5523–5532.
CAS | PubMed |
open url image1

Sambrook J , Fritsch EF , Maniatis T (1989) ‘Molecular cloning: a laboratory manual.’ 2nd edn. (Cold Spring Harbor Laboratory Press: New York)

Savaldi-Goldstein S, Peto C, Chory J (2007) The epidermis both drives and restricts plant shoot growth. Nature 446, 199–202.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y (2001) The asymmetric leaves2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128, 1771–1783.
CAS | PubMed |
open url image1

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. Proceedings of the National Academy of Sciences of the United States of America 99, 4730–4735.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wang XQ, Xu WH, Ma LG, Fu ZM, Deng XW, Li JY, Wang YH (2006) Requirement of KNAT1/BP for the development of abscission zones in Arabidopsis thaliana. Journal of Integrative Plant Biology 48, 15–26.
CAS |
open url image1

Wille AC, Lucas WJ (1984) Ultrastructural and histochemical studies on guard cells. Planta 160, 129–142.
Crossref | GoogleScholarGoogle Scholar | open url image1

Xu L, Xu Y, Dong A, Sun Y, Pi L, Xu Y, Huang H (2003) Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130, 4097–4107.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1