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POLTERGEIST and POLTERGEIST-LIKE1 are essential for the maintenance of post-embryonic shoot and root apical meristems as revealed by a partial loss-of-function mutant allele of pll1 in Arabidopsis

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Abstract

Background

POLTERGEIST (POL) and POL-LIKE1 (PLL1) encoding related protein phosphatase 2Cs are essential for the establishment of both shoot and root meristems during embryogenesis. As the strong pol pll1 are seedling-lethal due to the lack of hypocotyl vasculature, the roles of POL/PLL1 for the post-embryonic development is difficult to be assessed.

Objective

To prepare a weak pol pll1 double mutant that are able to produce post-embryonic organs.

Methods

Several T-DNA insertion mutants of pll1 were crossed to pol-6 for the preparation of weak pol pll1. To understand the epistatic interactions between POL/PLL1 and CLAVATAs, the phenotypes of clvs pol pll1 were assessed and the expression patterns of stem cell markers were examined in pol pll1. POLpro:PLL1-GFP expression was examined during the embryogenesis with confocal microscopy.

Results

We isolated a pll1-3 (S544N) allele and prepared a weak pol-6 pll1-3. About 5% of pol-6 pll1-3 seedlings continued the post-embryonic development displaying short roots with reduced root meristem, wuschel-like adventitious phyllotaxis, and defective flowers lacking carpel. The clv1, clv2, and clv3 phenotypes led by enlarged shoot meristems were almost completely suppressed in the pol-6 pll1-3. POL/PLL1 were required for the indeterminate floral organ development displayed by agamous. PLL1-GFP asymmetrically localized in the shootward sides of columella cells and increased the size of distal root meristem region by enhancing the WUS-RELATED HOMEOBOX 5 expression suggesting that PLL1 might provide the stem cells and progenies with proper positional information for the asymmetric cell divisions.

Conclusion

Together, POL/PLL1 are required for the maintenance of stem cell pools for the post-embryonic development in Arabidopsis.

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Abbreviations

ACR4 :

ARABIDOPSIS CRINKLY4

AG :

AGAMOUS

AS :

ASYMMETRIC LEAVES

BAM :

BARELY ANY MERISTEM

CLE :

CLV3/ENDOSPERM SURROUNDING REGION

CLV :

CLAVATA

CRN :

CORYNE

CSC:

Columella stem cell

CUC :

CUP SHAPED COTYLEDON

OC:

Organizing center

PLL1 :

POLTERGEIST- LIKE1

POL :

POLTERGEIST

QC:

Quiescent center

STM :

SHOOT MERISTEMLESS

WOX :

WUS-RELATED HOMEOBOX

WUS :

WUSCHEL

References

  • Aida M, Ishida T, Tasaka M (1999) Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126:1563–1570

    CAS  PubMed  Google Scholar 

  • Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152:166–176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408:967

    CAS  PubMed  Google Scholar 

  • Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129:1957–1965

    CAS  PubMed  Google Scholar 

  • Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–2067

    CAS  Google Scholar 

  • Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122:1567–1575

    CAS  PubMed  Google Scholar 

  • Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585

    CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    CAS  PubMed  Google Scholar 

  • de Jong M, Leyser O (eds) (2012) Developmental plasticity in plants. In: Cold Spring Harbor symposia on quantitative biology. Cold Spring Harbor Laboratory Press, New York, pp 63–73. https://doi.org/10.1101/sqb.2012.77.014720

    CAS  PubMed  Google Scholar 

  • DeYoung BJ, Clark SE (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180:895–904

    CAS  PubMed  PubMed Central  Google Scholar 

  • DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16

    CAS  PubMed  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    PubMed  Google Scholar 

  • Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10:967–979

    CAS  PubMed  Google Scholar 

  • Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132

    CAS  PubMed  Google Scholar 

  • Gagne JM, Clark SE (2010) The Arabidopsis stem cell factor POLTERGEIST is membrane localized and phospholipid stimulated. Plant Cell 22:729–743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geldner N, Richter S, Vieten A, Marquardt S, Torres-Ruiz RA, Mayer U, Jürgens G (2004) Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131:389–400

    CAS  PubMed  Google Scholar 

  • Groß-Hardt R, Lenhard M, Laux T (2002) WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes Dev 16:1129–1138

    PubMed  PubMed Central  Google Scholar 

  • Hamann T, Benkova E, Bäurle I, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–478

    CAS  PubMed  Google Scholar 

  • Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–1933

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ (2010) WOX4 promotes procambial development. Plant Physiol 152:1346–1356

    CAS  PubMed  Google Scholar 

  • Kanrar S, Onguka O, Smith HM (2006) Arabidopsis inflorescence architecture requires the activities of KNOX-BELL homeodomain heterodimers. Planta 224:1163–1173

    CAS  PubMed  Google Scholar 

  • Lee MM, Schiefelbein J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99:473–483

    CAS  PubMed  Google Scholar 

  • Lee MM, Schiefelbein J (2002) Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14:611–618

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lenhard M, Jürgens G, Laux T (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 129:3195–3206

    CAS  PubMed  Google Scholar 

  • Leung J, Bouvier-Durand M, Morris P-C, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264:1448–1452

    CAS  PubMed  Google Scholar 

  • Lita PY, Miller AK, Clark SE (2003) POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Curr Biol 13:179–188

    Google Scholar 

  • Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803

    CAS  PubMed  Google Scholar 

  • Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035

    CAS  PubMed  Google Scholar 

  • Malamy JE, Benfey PN (1997) Analysis of SCARECROW expression using a rapid system for assessing transgene expression in Arabidopsis roots. Plant J 12:957–963

    CAS  PubMed  Google Scholar 

  • Mayer A, Wickner W, Haas A (1996) Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede docking and fusion of yeast vacuoles. Cell 85:83–94

    CAS  PubMed  Google Scholar 

  • Müller R, Bleckmann A, Simon R (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–946

    PubMed  PubMed Central  Google Scholar 

  • Nimchuk ZL, Tarr PT, Ohno C, Qu X, Meyerowitz EM (2011) Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr Biol 21:345–352

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T (2007) ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. Plant J 50:935–949

    CAS  PubMed  Google Scholar 

  • Pi L, Aichinger E, van der Graaff E, Llavata-Peris CI, Weijers D, Hennig L, Groot E, Laux T (2015) Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev Cell 33:576–588

    CAS  PubMed  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811

    CAS  PubMed  Google Scholar 

  • Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644

    CAS  PubMed  Google Scholar 

  • Sessions A, Weigel D, Yanofsky MF (1999) The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J 20:259–263

    CAS  PubMed  Google Scholar 

  • Song S-K, Clark SE (2005) POL and related phosphatases are dosage-sensitive regulators of meristem and organ development in Arabidopsis. Dev Biol 285:272–284

    CAS  PubMed  Google Scholar 

  • Song S-K, Lee MM, Clark SE (2006) POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells. Development 133:4691–4698

    CAS  PubMed  Google Scholar 

  • Song S-K, Hofhuis H, Lee MM, Clark SE (2008) Key divisions in the early Arabidopsis embryo require POL and PLL1 phosphatases to establish the root stem cell organizer and vascular axis. Dev Cell 15:98–109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914

    CAS  PubMed  Google Scholar 

  • Stahl Y, Grabowski S, Bleckmann A, Kühnemuth R, Weidtkamp-Peters S, Pinto KG, Kirschner GK, Schmid JB, Wink RH, Hülsewede A (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23:362–371

    CAS  PubMed  Google Scholar 

  • Weigel D, Jürgens G (2002) Stem cells that make stems. Nature 415:751

    CAS  PubMed  Google Scholar 

  • Xiang C, Han P, Lutziger I, Wang K, Oliver DJ (1999) A mini binary vector series for plant transformation. Plant Mol Biol 40:711–717

    CAS  PubMed  Google Scholar 

  • Xue T, Wang D, Zhang S, Ehlting J, Ni F, Jakab S, Zheng C, Zhong Y (2008) Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genom 9:550

    Google Scholar 

  • Yadav RK, Perales M, Gruel J, Girke T, Jönsson H, Reddy GV (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:2025–2030

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35

    CAS  PubMed  Google Scholar 

  • Yu L, Simon EJ, Trotochaud AE, Clark SE (2000) POLTERGEIST functions to regulate meristem development downstream of the CLAVATA loci. Development 127:1661–1670

    CAS  PubMed  Google Scholar 

  • Zhang Z, Tucker E, Hermann M, Laux T (2017) A molecular framework for the embryonic initiation of shoot meristem stem cells. Dev Cell 40(264–277):e264

    Google Scholar 

  • Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, Yan A, Kay SA, Meyerowitz EM (2015) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 517:377

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by a Grant from Woo Jang Choon project (Grant number, PJ01093905 to MML) of the Rural Development Administration, Republic of Korea., research funds from Chosun University 2014 (K206888001) and 2015 (K206888002) to S.S.

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Author notes

  1. Sang-Kee Song and Young Bin Yun contributed equally to the article.

Authors and Affiliations

  1. Department of Biology, Chosun University, Gwangju, 61452, Korea

    Sang-Kee Song & Young Bin Yun

  2. Department of Systems Biology, Yonsei University, 50 Yonsei-ro, Seoul, 03722, Korea

    Myeong Min Lee

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  1. Sang-Kee Song
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Song, SK., Yun, Y.B. & Lee, M.M. POLTERGEIST and POLTERGEIST-LIKE1 are essential for the maintenance of post-embryonic shoot and root apical meristems as revealed by a partial loss-of-function mutant allele of pll1 in Arabidopsis. Genes Genom 42, 107–116 (2020). https://doi.org/10.1007/s13258-019-00894-8

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