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Multi-tasking of SERK-like kinases in plant embryogenesis, growth, and development: current advances and biotechnological applications

  • Vijay Kumar
  • Johannes Van StadenEmail author
Review

Abstract

In plants, exogenous signals play a vital role in cell metabolism modification leading to growth and defense responses. The SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) belongs to a family of leucine-rich repeat receptor-like kinases (LRR-RLKs), involved in cell-to-embryo-transition, plant environmental responses, and plant development. SERKs interact with various ligand-binding receptors with complex-signaling networks and appear to function in diverse biological processes in plant development and physiology. The present review explores the current status of the role of SERK genes as candidate marker during plant embryogenesis. Furthermore, we describe recent advances in newly identified SERK functions and provide novel insights into different biotechnological advances. The recent advancements in newly identified SERK will help to unlock the long-standing mysteries of different biological and molecular mechanisms of plant cells.

Keywords

Biotechnological applications Biological mechanism Embryogenesis Plant growth SERK 

Abbreviations

ABA

Abscisic acid

ABI1

ABA-insensitive1

BA

N6-Benzyladenine

BIK1

Botrytis-induced kinase 1

BL

Brassinolide

BRI1

Brassinosteroid insensitive1

BiFC

Bimolecular fluorescence complementation

CLE

Clavata3/endosperm surrounding region

CSP

Cold shock protein

Co-IP

Co-immunoprecipitation

CNGC17

Cyclic nucleotide-gated channel17

2,4-D

2,4-Dichlorophenoxyacetic acid

ER

Erecta

ERF1

Ethylene response factor1

ERL1

Erecta like1

EPF1

Epidermal patterning factor1

EMS1

Excess micro-sporocytes1

FLS2

Flagellin sensing2

FRET

Forster resonance energy transfer

GUS

β-Glucuronidase

IDA

Inflorescence deficient in abscission

IZE

Immature zygotic embryos

INS

Internodal segment

LRR-RLKs

Leucine-rich repeat receptor-like kinases

NAA

Naphthalene-acetic acid

OST1

Open stomata1

PAMPs

Pathogen-associated molecular patterns

PLB

Protocorm-like body

PR1

Pathogenesis-related protein1

PAD4

Phytoalexin deficient4

PP2A

Protein phosphatase 2A

PRRs

Pattern recognition receptors

PUB

Plant U-box

RGF

Root meristem growth factor

RLKs

Resident receptor-like kinases

RLPs

Resident receptor-like Proteins

ROS

Reactive oxygen species

SAM

Shoot apical meristem

SE

Somatic embryogenesis

SERK

Somatic embryogenesis receptor-like kinase

TD1

Twisted dwarf 1

TPD

Tapetum determinant1

TMM

Too many mouth

VIGS

Virus-induced gene silencing

Notes

Acknowledgements

VK wish to acknowledge the Claude Leon Foundation and University of KwaZulu-Natal, South Africa for financial support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aan den Toorn M, Albrecht C, de Vries S (2015) On the origin of SERKs: bioinformatics analysis of the somatic embryogenesis receptor kinases. Mol Plant 8:762–782PubMedCrossRefPubMedCentralGoogle Scholar
  2. Albert I, Böhm H, Albert M, Feiler CE, Imkampe J, Wallmeroth N, Brancato C, Raaymakers TM, Oome S, Zhang H, Krol E, Grefen C, Gust AA, Chai J, Hedrich R, Van den Ackerveken G, Thorsten Nürnberger T (2015) An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity. Nat Plants 1:15140PubMedCrossRefPubMedCentralGoogle Scholar
  3. Albertini E, Marconi G, Reale L, Barcaccia G, Porceddu A, Ferranti F, Falcinelli M (2005) SERK and APOSTART. Candidate Gene for Apomixis in Poa pratensis. Plant Physiol 138:2185–2199PubMedPubMedCentralCrossRefGoogle Scholar
  4. Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana somatic embryogenesisreceptor-like kinases 1 and 2 control male sporogenesis. Plant Cell 17:3337–3349PubMedPubMedCentralCrossRefGoogle Scholar
  5. Albrecht C, Boutrot F, Segonzac C, Schwessinger B, GimenezIbanez S, Chinchilla D, Rathjen JP, de Vries SC, Zipfel C (2012) Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc Natl Acad Sci USA 109:303–308PubMedCrossRefPubMedCentralGoogle Scholar
  6. Baudino S, Hansen S, Brettschneider R, Hecht VF, Dresselhaus T, Lörz H, Dumas C, Rogowsky PM (2001) Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family. Planta 213:1–10PubMedCrossRefPubMedCentralGoogle Scholar
  7. Becker D, Hoth S, Ache P, Wenkel S, Roelfsema MR, Meyerhoff O, Hartung W, Hedrich R (2003) Regulation of the ABA-sensitive Arabidopsis potassium channel gene GORK in response to water stress. FEBS Lett 554:119–126PubMedCrossRefPubMedCentralGoogle Scholar
  8. Belkhadir Y, Jaillais Y, Epple P, Balsemão-Pires E, Dangl JL, Chory J (2012) Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci USA 109:297–302PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bell EM, Lin WC, Husbands AY, Yu L, Jaganatha V, Jablonska B, Mangeon A, Neff MM, Girke T, Springer PS (2012) Arabidopsis LATERAL ORGAN BOUNDARIES negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci USA 109:21146–21151PubMedCrossRefPubMedCentralGoogle Scholar
  10. Blaum BS, Mazzotta S, Nöldeke ER, Halter T, Madlung J, Kemmerling B, Stehle T (2014) Structure of the pseudokinase domain of BIR2, a regulator of BAK1-mediated immune signaling in Arabidopsis. J Struct Biol 186:112–121PubMedCrossRefPubMedCentralGoogle Scholar
  11. Brandt B, Hothorn M (2016) SERK co-receptor kinases. Curr Biol 26:225–226CrossRefGoogle Scholar
  12. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, Aalen RB (2003) Inflorescence deficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15:2296–2307PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chaiwanon J, Garcia VJ, Cartwright H, Sun Y, Wang ZY (2016) Immunophilin-like FKBP42/twisted dwarf1 interacts with the receptor kinase BRI1 to regulate brassinosteroid signaling in Arabidopsis. Mol Plant 9:593–600PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chen X, Zuoa S, Schwessingera B, Cherna M, Canlasa PE, Ruana D, Zhou X, Wang J, Daudia A, Petzold CJ, Heazlewood JL, Ronald PC (2014) An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors. Mol Plant 7:874–892PubMedPubMedCentralCrossRefGoogle Scholar
  15. Cheng Y, Zhu W, Chen Y, Ito S, Asami T, Wang X (2014) Brassinosteroids control root epidermal cell fate via direct regulation of a MYB-bHLH-WD40 complex by GSK3-like kinases. Elife 3:e02525PubMedCentralCrossRefGoogle Scholar
  16. Cheung AY, Wu HM (2015) Stomatal patterning: SERKs put the mouths in their right place. Curr Biol 25:827–844CrossRefGoogle Scholar
  17. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nat 448:497–500CrossRefGoogle Scholar
  18. Chugh A, Khurana P (2002) Gene expression during somatic embryogenesis—recent advances. Curr Sci 86:715–730Google Scholar
  19. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585PubMedPubMedCentralCrossRefGoogle Scholar
  20. Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451PubMedPubMedCentralCrossRefGoogle Scholar
  21. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis somatic embryogenesis receptor kinases1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cueva A, Concia L, Cella R (2012) Molecular characterization of a Cyrtochilum loxense somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Cell Rep 31:1129–1139PubMedCrossRefPubMedCentralGoogle Scholar
  23. Du J, Yin H, Zhang S, Wei Z, Zhao B, Zhang J, Gou X, Lin H, Li J (2012) Somatic embryogenesis receptor kinases control root development mainly via brassinosteroid-independent actions in Arabidopsis thaliana. J Integ Plant Biol 54:388–399CrossRefGoogle Scholar
  24. Du J, Verzaux E, Chaparro-Garcia A, Bijsterbosch G, Keizer LCP, Zhou J, Liebrand TWH, Xie C, Govers F, Robatzek S, van der Vossen EAG, Jacobsen E, Visser RGF, Kamoun S, Vleeshouwers VGAA (2015) Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat Plants 1:15034PubMedCrossRefPubMedCentralGoogle Scholar
  25. Fan M, Wang M, Bai MY (2016) Diverse roles of SERK family genes in plant growth, development and defense response. Sci China Life Sci 59:889–896PubMedCrossRefPubMedCentralGoogle Scholar
  26. Fisher K, Turner S (2007) PXY, a receptor-like kinase essential form maintaining polarity during plant vascular-tissue development. Curr Biol 17:1061–1066PubMedCrossRefPubMedCentralGoogle Scholar
  27. Gao X, Li F, Li M, Kianinejad AS, Dever JK, Wheeler TA, Li Z, He P, Shan L (2013) Cotton GhBAK1 mediates Verticillium Wilt resistance and cell death. J Integr Plant Biol 55:586–596PubMedPubMedCentralCrossRefGoogle Scholar
  28. Ge XX, Fan GE, Chai LJ, Guo WW (2010) Cloning, molecular characterization and expression analysis of a SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE gene (CitSERK1-Like) in valencia sweet orange. Acta Physiol Plant 32:1197–1207CrossRefGoogle Scholar
  29. Gendron JM, Liu JS, Fan M, Bai MY, Wenkel S, Springer PS, Barton MK, Wang ZY (2012) Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proc Natl Acad Sci USA109:21152–21157CrossRefGoogle Scholar
  30. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229PubMedPubMedCentralCrossRefGoogle Scholar
  31. Gou X, Yin H, He K, Du J, Yi J, Xu S, Lin H, Clouse SD, Li J (2012) Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet 8:e1002452PubMedPubMedCentralCrossRefGoogle Scholar
  32. Gudesblat GE, Russinova E (2011) Plants grow on brassinosteroids. Curr Opin Plant Biol 14:530–537PubMedCrossRefPubMedCentralGoogle Scholar
  33. Gudesblat GE, Schneider-Pizoń J, Betti C, Mayerhofer J, Vanhoutte I, van Dongen W, Boeren S, Zhiponova M, de Vries S, Jonak C, Russinova E (2012) SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat Cell Biol 14:548–554PubMedCrossRefPubMedCentralGoogle Scholar
  34. Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138:839–848PubMedPubMedCentralCrossRefGoogle Scholar
  35. Halter T, Imkampe J, Mazzotta S, Wierzba M, Postel S, Bücherl C, Kiefer C, Stahl M, Chinchilla D, Wang X, Nürnberger T, Zipfel C, Clouse S, Borst JW, Boeren S, de Vries SC, Tax F, Kemmerling B (2014) The Leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Curr Biol 24:134–143PubMedCrossRefPubMedCentralGoogle Scholar
  36. Hatsuagi N, Igarashi D, Mase K, Lu Y, Tsuda Y, Chakravarthy S, Wei HL, Foley JW, Collmer A, Glazebrook J, Katagiri F (2017) A plant effector-triggered immunity signaling sector is inhibited by pattern triggered immunity. EMBO J 36:2758–2769CrossRefGoogle Scholar
  37. He K (2008) Functional analyses of somatic embryogenesis receptor-like kinase family in multiple signaling pathways in Arabidopsis. Ph.D. Thesis, The University of Oklahoma, Norman, 143Google Scholar
  38. He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, Russell SD, Li J (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr Biol 17:1109–1115PubMedCrossRefGoogle Scholar
  39. Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis somatic embryogenesis receptor kinase 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816PubMedPubMedCentralCrossRefGoogle Scholar
  40. Holton N, Nekrasov V, Ronald PC, Zipfel C (2015) The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signalling components in monocots and dicots. PLoS Pathog 11:e1004602PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hu H, Brown PH (1994) Localization of boron in cell walls of squash and tobacco and its association with pectin. Plant Physiol 105:681–689PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively regulates somatic embryogenesis of cultured cells and host defense response against fungal infection. Planta 222:107–117PubMedCrossRefPubMedCentralGoogle Scholar
  43. Huang X, Lu XY, Zhao JT, Chen JK, Dai XM, Xiao W, Chen YP, Chen YF, Huang XL (2010) MaSERK1 gene expression associated with somatic embryogenic competence and disease resistance response in banana (Musa spp.). Plant Mol Biol Rep 28:309–316CrossRefGoogle Scholar
  44. Huang YW, Tsai YJ, Chen FC (2014) Characterization and expression analysis of somatic embryogenesis receptor-like kinase genes from Phalaenopsis. Genet Mol Res 13:10690–10703PubMedCrossRefPubMedCentralGoogle Scholar
  45. Hubbard KE, Siegel RS, Valerio G, Brandt B, Schroeder JI (2012) Abscisic acid and CO2 signalling via calcium sensitivity priming in guard cells, new CDPK mutant phenotypes and a method for improved resolution of stomatal stimulus-response analyses. Ann Bot 109:5–17PubMedCrossRefPubMedCentralGoogle Scholar
  46. Hutten SJ, Hamers DS, Aan den Toorn M, van Esse W, Nolles A, Bücherl CA, de Vries SC, Hohlbein J, Borst JW (2017) Visualization of BRI1 and SERK3/BAK1 nanoclusters in Arabidopsis roots. PloS One 12:e0169905PubMedPubMedCentralCrossRefGoogle Scholar
  47. Jha P, Kumar V (2018) BABY BOOM (BBM): a candidate transcription factor gene in plant biotechnology. Biotechnol Lett 40:1467–1475PubMedCrossRefPubMedCentralGoogle Scholar
  48. Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc Natl Acad Sci USA 105:2220–2225PubMedCrossRefPubMedCentralGoogle Scholar
  49. Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, de Vries S (2006) The Arabidopsis somatic embryogenesis receptor-like kinase1 protein complex includes brassinosteroid-insensitive1. Plant Cell 18:626–638PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA, Mengiste T, Betsuyaku S, Parker JE, Müssig C, Thomma BP, Albrecht C, de Vries SC, Hirt H, Nürnberger T (2007) The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr Biol 17:1112–1116CrossRefGoogle Scholar
  51. Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704PubMedCrossRefPubMedCentralGoogle Scholar
  52. Kim TW, Michniewicz M, Bergmann DC, Wang ZY (2012) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482:419–422PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kumar V, Van Staden J (2017) New insights into plant somatic embryogenesis: an epigenetic view. Acta Physiol Plant 39:194CrossRefGoogle Scholar
  54. Kutschmar A, Rzewuski G, Stührwohldt N, Beemster GTS, Inzé D, Sauter M (2009) PSK-α promotes root growth in Arabidopsis. New Phytol 181:820–831PubMedCrossRefPubMedCentralGoogle Scholar
  55. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP, Smoker M, Rallapalli G, Thomma BPHJ, Staskawicz B, Jones JDG, Zipfel C (2010) Interfamily transfer of a plant patternrecognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28:365–369PubMedCrossRefPubMedCentralGoogle Scholar
  56. Ladwig F, Dahlke RI, Stührwohldt N, Hartmann J, Harter K, Sauter M (2015) Phytosulfokine regulates growth in Arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1. Plant Cell 27:1718–1729PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM, McAbee JM, Sarikaya M, Tamerler C, Torii KU (2012) Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev 26:126–136PubMedPubMedCentralCrossRefGoogle Scholar
  58. Li J (2010) Multi-tasking of somatic embryogenesis receptor-like protein kinases. Curr Opin Plant Biol 13:509–514PubMedCrossRefPubMedCentralGoogle Scholar
  59. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938PubMedPubMedCentralCrossRefGoogle Scholar
  60. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222PubMedPubMedCentralCrossRefGoogle Scholar
  61. Li X, Fang YH, Han JD, Bai SN, Rao GY (2015) Isolation and characterization of a novel somatic embryogenesis receptor kinase gene expressed in the fern Adiantum capillus-veneris during shoot regeneration in vitro. Plant Mol Biol Rep 33:638–647CrossRefGoogle Scholar
  62. Li Z, Wang Y, Huang J, Ahsan N, Biener G, Paprocki J, Thelen JJ, Raicu V, Zhao D (2017) Two SERK receptor-like kinases interact with EMS1 to control anther cell fate determination. Plant Physiol 173:1326–1337Google Scholar
  63. Liebrand TW, van den Burg HA, Joosten MH (2014) Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19:123–132PubMedCrossRefPubMedCentralGoogle Scholar
  64. Liljegren SJ (2012) Organ abscission: exit strategies require signals and moving traffic. Curr Opin Plant Biol 15:670–676PubMedCrossRefPubMedCentralGoogle Scholar
  65. Lin W, Lia B, Lu D, Chen S, Zhu N, He P, Shan L (2014) Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. Proc Natl Acad Sci USA111:3632–3637CrossRefGoogle Scholar
  66. Liu J, Chen S, Chen L, Zhou Q, Wang M, Feng D, Li JF, Wang J, Wang HB, Liu B (2017) BIK1 cooperates with BAK1 to regulate constitutive immunity and cell death in Arabidopsis. J Integr Plant Biol 59:234–239PubMedCrossRefPubMedCentralGoogle Scholar
  67. Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–1442PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ma J, He Y, Hu Z, Xu W, Xia J, Guo C, Lin S, Cao L, Chen C, Wu C, Zhang J (2012a) Characterization and expression analysis of AcSERK2, a somatic embryogenesis and stress resistance related gene in pineapple. Gene 500:115–123PubMedCrossRefPubMedCentralGoogle Scholar
  69. Ma J, He YH, Wu CH, Liu HP (2012b) Cloning and molecular characterization of a SERK gene transcriptionally induced during somatic embryogenesis in Ananas comosus cv. Shenwan. Plant Mol Biol Rep 30:195–203CrossRefGoogle Scholar
  70. Ma J, He Y, Hu Z, Xu W, Xia J, Guo C, Lin S, Chen C, Wu C, Zhang J (2014) Characterization of the third SERK gene in pineapple (Ananas comosus) and analysis of its expression and autophosphorylation activity in vitro. Genet Mol Biol 37:530–539PubMedPubMedCentralCrossRefGoogle Scholar
  71. Ma X, Xu G, He P, Shan L (2016) SERKing coreceptors for receptors. Trends Plant Sci 21:1017–1033PubMedCrossRefPubMedCentralGoogle Scholar
  72. Mahdavi-Darvari F, Noor NM, Ismanizan I (2015) Epigenetic regulation and gene markers as signals of early somatic embryogenesis. Plant Cell Tissue Organ Cult 120:407–422CrossRefGoogle Scholar
  73. Mantelin S, Peng HC, Li B, Atamian HS, Takken FL, Kaloshian I (2011) The receptor-like kinase SlSERK1 is required for Mi-1-mediated resistance to potato aphids in tomato. Plant J 67:459–471PubMedCrossRefPubMedCentralGoogle Scholar
  74. Matsubayashi Y (2014) Posttranslationally modified small-peptide signals in plants. Annu Rev Plant Biol 65:385–413PubMedCrossRefPubMedCentralGoogle Scholar
  75. Meng X, Chen X, Mang H, Liu C, Yu X, Gao X, Torii KU, He P, Shan L (2015) Differential function of Arabidopsis SERK family receptor-like kinases in stomatal patterning. Curr Biol 25:2361–2372PubMedPubMedCentralCrossRefGoogle Scholar
  76. Meng X, Zhou J, Tang J, Li B, de Oliveira MV, Chai J, He P, Shan L (2016) Ligand-induced receptor-like kinase complex regulates floral organ abscission in Arabidopsis. Cell Rep 14:1330–1338PubMedPubMedCentralCrossRefGoogle Scholar
  77. Merkle SA, Parrott WA, Williams EG (1990) Applications of somatic embryogenesis and embryo cloning. Dev Crop Sci 19:67–101CrossRefGoogle Scholar
  78. Miyashima S, Sebastian J, Lee JY, Helariutta Y (2013) Stem cell function during plant vascular development. EMBO J32:178–193Google Scholar
  79. Monda K, Negi J, Iio A, Kusumi K, Kojima M, Hashimoto M, Sakakibara H, Iba K (2011) Environmental regulation of stomatal response in the Arabidopsis Cvi-0 ecotype. Planta 234:555–563PubMedCrossRefPubMedCentralGoogle Scholar
  80. Murphy E, Smith S, De Smet I (2012) Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24:3198–3217PubMedPubMedCentralCrossRefGoogle Scholar
  81. Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212PubMedPubMedCentralCrossRefGoogle Scholar
  82. Niederhuth CE, Cho SK, Seitz K, Walker JC (2013) Letting go is never easy: abscission and receptor-like protein kinases. J Integr Plant Biol 55:1251–1263PubMedCrossRefPubMedCentralGoogle Scholar
  83. Nodine MD, Yadegari R, Tax FE (2007) RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Dev Cell 12:943–956PubMedCrossRefPubMedCentralGoogle Scholar
  84. Nogler G (1984) Gametophytic apomixis. In: Johri BM (ed) Embryology of An-giosperms. Springer, Berlin, pp 475–518CrossRefGoogle Scholar
  85. Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiol 133:218–230PubMedPubMedCentralCrossRefGoogle Scholar
  86. Nolan KE, Kurdyukov S, Rose RJ (2009) Expression of the somatic embryogenesis receptor-like linase1 (SERK1) gene is associated with developmental change in the life cycle of the model legume Medicago truncatulata. J Exp Bot 60:1759–1771PubMedPubMedCentralCrossRefGoogle Scholar
  87. Nolan KE, Kurdyukov S, Rose RJ (2011) Characterisation of the legume SERK-NIKgene superfamily including splice variants: Implications for development and defence. BMC Plant Biol 11:44PubMedPubMedCentralCrossRefGoogle Scholar
  88. Oh MH, Wang X, Wu X, Zhao Y, Clouse SD, Huber SC (2010) Autophosphorylation of Tyr-610 in the receptor kinase BAK1 plays a role in brassinosteroid signalling and basal defense gene expression. Proc Natl Acad Sci USA 107:17827–17832PubMedCrossRefPubMedCentralGoogle Scholar
  89. Oliveira EJ, Koehler AD, Rocha DI, Vieira LM, Pinheiro MV, Matos EM, Cruz AC, Silva TC, Tanaka FA, Nogueira FTS, Otoni W (2017) Morpho-histological, histochemical, and molecular evidences related to cellular reprogramming during somatic embryogenesis of the model grass Brachypodium distachyon. Protoplasma 254:2017–2034PubMedCrossRefPubMedCentralGoogle Scholar
  90. Ou Y, Lu X, Zi Q, Xun Q, Zhang J, Wu Y, Shi H, Wei Z, Zhao B, Zhang X, He K, Gou X, Li C, Li J (2016) RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana. Cell Res 26:686–698PubMedPubMedCentralCrossRefGoogle Scholar
  91. Park HS, Ryu HY, Kim BH, Kim SY, Yoon IS, Nam KH (2011) A subset of OsSERK genes, including OsBAK1, affects normal growth and leaf development of rice. Mol Cells 32:561–569PubMedPubMedCentralCrossRefGoogle Scholar
  92. Peng HC, Kaloshian I (2014) The tomato leucine-rich repeat receptor-like kinases SlSERK3A and SlSERK3B have overlapping functions in bacterial and nematode innate immunity. PLoS One 9:e93302PubMedPubMedCentralCrossRefGoogle Scholar
  93. Pérez M, Cañal MJ, Toorop PE (2015) Expression analysis of epigenetic and abscisic acid-related genes during maturation of Quercus suber somatic embryos. Plant Cell Tissue Organ Cult 121:353–366CrossRefGoogle Scholar
  94. Pérez-Núñez M, Souza R, Sáenz L, Chan J, Zúñiga-Aguilar J, Oropeza C (2009) Detection of a SERK-like gene in coconut in vitro cultures and analysis of its expression during the formation of embryogenic callus and somatic embryos. Plant Cell Rep 28:11–19PubMedCrossRefPubMedCentralGoogle Scholar
  95. Pilarska M, Malec P, Salaj J, Bartnicki F, Konieczny R (2016) High expression of somatic embryogenesis receptor-like kinase coincides with initiation of various developmental pathways in in vitro culture of Trifolium nigrescens. Protoplasma 253:345–355PubMedCrossRefPubMedCentralGoogle Scholar
  96. Podio M, Felitti SA, Siena LA, Delgado L, Mancini M, Seijo JG, Gonzalez AM, Pessino SC, Ortiz JPA (2014) Characterization and expression analysis of SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) genes in sexual and apomictic Paspalum notatum. Plant Mol Biol 84:479–495PubMedCrossRefPubMedCentralGoogle Scholar
  97. Postel S, Kufner I, Beuter C, Mazzotta S, Schwedt A, Borlotti A, Halter T, Kemmerling B, Nurnberger T (2010) The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur J Cell Biol 89:169–174PubMedCrossRefPubMedCentralGoogle Scholar
  98. Postma J, Liebrand TW, Bi G, Evrard A, Bye RR, Mbengue M, Kuhn H, Joosten MH, Robatzek S (2016) Avr4 promotes Cf-4 receptor-like protein association with the BAK1/SERK3 receptor-like kinase to initiate receptor endocytosis and plant immunity. New Phytol 210:627–642PubMedCrossRefPubMedCentralGoogle Scholar
  99. Quiroz-Figueroa FR, Rojas-Herrera R, Galaz-Avalos RM, Loyola-Vargas VM (2006) Embryo production through somatic embryogenesis can be used to study cell differentiation in plants. Plant Cell Tissue Organ Cult 86:285–301CrossRefGoogle Scholar
  100. Rocha DI, Pinto DLP, Vieira LM, Tanaka FAO, Dornelas MC, Otoni WC (2015) Cellular and molecular changes associated with competence acquisition during passion fruit somatic embryogenesis: ultrastructural characterization and analysis of SERK gene expression. Protoplasma 253:595–609PubMedCrossRefPubMedCentralGoogle Scholar
  101. Rocha DI, Monte-Belo CC, Aizza LCB, Dornelas MC (2016) A passion fruit putative ortholog of the somatic embryogenesis receptor kinase1 gene is expressed throughout the in vitro de novo shoot organogenesis developmental program. Plant Cell Tissue Organ Cult 125:107–117CrossRefGoogle Scholar
  102. Rojas-Herrera R, Quiroz-Figueroa FR, Monforte-González M, Sánchez-Teyer F, Loyola-Vargas VM (2002) Differential gene expression during somatic embryogenesis in Coffea arabica L., revealed by RT-PCR differential display. Mol Biotechnol 21:43–50CrossRefGoogle Scholar
  103. Roux M, Schwessingera B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tör M, de Vries SC, Zipfel C (2011) The Arabidopsis leucine-rich repeat receptor–like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440–2455PubMedPubMedCentralCrossRefGoogle Scholar
  104. Rupps A, Raschke J, Rümmler M, Linke B, Zoglauer K (2016) Identification of putative homologs of Larix decidua to babyboom (BBM), leafy cotyledon1 (LEC1), wuschel-related homeobox2 (WOX2) and somatic embryogenesis receptor-like KINASE (SERK) during somatic embryogenesis. Planta 243:473–488PubMedCrossRefPubMedCentralGoogle Scholar
  105. Sakamoto T, Deguchi M, Brustolini OJ, Santos AA, Silva FF, Fontes EPB (2012) The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol 12:229PubMedPubMedCentralCrossRefGoogle Scholar
  106. Salaj J, Recklinghausen IR, Hecht V, de Vries SC, Schel JHN, van Lammeren AAM (2008) AtSERK1 expression precedes and coincides with early somatic embryogenesis in Arabidopsis thaliana. Plant Physiol Biol 46:709–714Google Scholar
  107. Santa-Catarina C, Hanai LR, Dornelas MC, Viana AM, Floh EIS (2004) SERK gene homolog expression, polyamines and amino acids associated with somatic embryogenic competence of Ocotea catharinensis Mez. (Lauraceae). Plant Cell Tissue Organ Cult 79:53–61CrossRefGoogle Scholar
  108. Santiago J, Brandt B, Wildhagen M, Hohmann U, Hothorn LA, Butenko MA, Hothorn M (2016) Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife 5:e15075PubMedPubMedCentralCrossRefGoogle Scholar
  109. Santos MO, Romanoa E, Yotoko KSC, Tinoco MLP, Dias BBA, Aragao FJL (2005) Characterization of the cacao somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Sci 168:723–729CrossRefGoogle Scholar
  110. Saur IML, Kadota Y, Sklenar J, Holton NJ, Smakowska E, Belkhadir Y, Zipfel C, Rathjen JP (2016) NbCSPR underlies age-dependent immune responses to bacterial cold shock protein in Nicotiana benthamiana. Proc Natl Acad Sci USA 113:3389–3394PubMedCrossRefPubMedCentralGoogle Scholar
  111. Savona M, Mattioli R, Nigro S, Falasca G, Della Rovere F, Costantino P, de Vries SC, Ruffoni B, Trovato M, Altamura MM (2012) Two SERK genes are markers of pluripotency in Cyclamen persicum Mill. J Exp Bot 63:471–488PubMedCrossRefPubMedCentralGoogle Scholar
  112. Schellenbaum P, Jacques A, Maillot P, Bertsch C, Mazet F, Farine S, Walter B (2008) Characterization of VvSERK1, VvSERK2, VvSERK3 and VvL1L genes and their expression during somatic embryogenesis of grapevine (Vitis vinifera L.). Plant Cell Rep 27:1799–1809PubMedCrossRefPubMedCentralGoogle Scholar
  113. Schmidt ED, Guzzo F, Toonen MA, de Vries SC (1997) A leucine rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062PubMedPubMedCentralGoogle Scholar
  114. Schoonbeek HJ, Wang HH, Stefanato FL, Craze M, Bowden S, Wallington E, Zipfel C, Ridout CJ (2015) Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat. New Phytol 206:606–613PubMedCrossRefPubMedCentralGoogle Scholar
  115. Schrader S, Kaldenhoff R, Richter G (1997) Expression of novel genes during somatic embryogenesis of suspension-cultured carrot cells (Daucus carota). J Plant Physiol 50:63–68CrossRefGoogle Scholar
  116. Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 285:9444–9451PubMedPubMedCentralCrossRefGoogle Scholar
  117. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A, Zipfel C (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet 7:17CrossRefGoogle Scholar
  118. Segonzac C, Macho AP, Sanmartín M, Ntoukakis V, Sánchez-Serrano JJ, Zipfel C (2014) Negative control of BAK1 by protein phosphatase 2A during plant innate immunity. EMBO J 33:2069–2079PubMedPubMedCentralCrossRefGoogle Scholar
  119. Shang Y, Dai C, Lee MM, Kwak JM, Nam KH (2016) BRI1-associated receptor kinase 1 regulates guard cell ABA signalling mediated by open stomata 1 in Arabidopsis. Mol Plant 9:447–460PubMedCrossRefPubMedCentralGoogle Scholar
  120. Sharma SK, Millam S, Hein I, Bryan GJ (2008) Cloning and molecular characterization of a potato SERK gene transcriptionally induced during initiation of somatic embryogenesis. Planta 228:319–330PubMedCrossRefPubMedCentralGoogle Scholar
  121. Shi YL, Guo SD, Zhang R, Meng ZG, Ren MZ (2014) The role of Somatic embryogenesis receptor-like kinase 1 in controlling pollen production of the Gossypium anther. Mol Biol Rep 41:411–422PubMedCrossRefPubMedCentralGoogle Scholar
  122. Shimada T, Hirabayashi T, Endo T, Fujii H, Kita M, Omura M (2005) Isolation and characterization of the somatic embryogenesis receptor-like kinase gene homologue (CitSERK1) from Citrus unshiu Marc. Sci Hort 103:233–238CrossRefGoogle Scholar
  123. Silva AT, Barduche D, do Livramento KG, Ligterink W, Paiva LV (2014) Characterization of a putative Serk-Like ortholog in embryogenic cell suspension cultures of Coffea arabica L. Plant Mol Biol Rep 32:176–184CrossRefGoogle Scholar
  124. Singh A, Khurana P (2017) Ectopic expression of Triticum aestivum SERK genes (TaSERKs) control plant growth and development in Arabidopsis. Sci Rep 7:12368PubMedPubMedCentralCrossRefGoogle Scholar
  125. Singla B, Tyagi AK, Khurana JP, Khurana P (2007) Analysis of expression profile of selected genes expressed during auxin-induced somatic embryogenesis in leaf base system of wheat (Triticum aestivum) and their possible interactions. Plant Mol Biol 65:677–692PubMedCrossRefPubMedCentralGoogle Scholar
  126. Somleva MN, Schmidt EDL, de Vries SC (2000) Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell tracking and by SERK expression. Plant Cell Rep 19:718–726CrossRefGoogle Scholar
  127. Song W, Liu L, Wang J, Wu Z, Zhang H, Tang J, Lin G, Wang Y, Wen X, Li W, Han Z, Guo H, Chai J (2016) Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Res 26:674–685PubMedPubMedCentralCrossRefGoogle Scholar
  128. Steiner N, Santa-Catarina C, Guerra MP, Cutri L, Dornelas MC, Floh EIS (2012) A gymnosperm homolog of somatic embryogenesis receptor-like kinase-1 (SERK1) is expressed during somatic embryogenesis. Plant Cell Tissue Organ Cult 109:41–50CrossRefGoogle Scholar
  129. Stenvik GE, Butenko MA, Urbanowicz BR, Rose JK, Aalen RB (2006) Overexpression of INFLORESCENCE DEFICIENT IN ABSCISSION activates cell separation in vestigial abscission zones in Arabidopsis. Plant Cell 18:1467–1476PubMedPubMedCentralCrossRefGoogle Scholar
  130. Stührwohldt N, Dahlke RI, Steffens B, Johnson A, Sauter M (2011) Phytosulfokine-α controls hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor. PLoS One 6:e21054PubMedPubMedCentralCrossRefGoogle Scholar
  131. Sugiyama Y, Uraji M, Watanabe-Sugimoto M, Okuma E, Munemasa S, Shimoishi Y, Nakamura Y, Mori IC, Iwai S, Murata Y (2012) FIA functions as an early signal component of abscisic acid signal cascade in Vicia faba guard cells. J Exp Bot 63:1357–1365PubMedCrossRefPubMedCentralGoogle Scholar
  132. Talapatra S, Ghoshal N, Raychaudhuri SS (2014) Molecular characterization, modeling and expression analysis of a somatic embryogenesis receptor kinase (SERK) gene in Momordica charantia L. during somatic embryogenesis. Plant Cell Tissue Organ Cult 116:271–283CrossRefGoogle Scholar
  133. Thomas C, Meyer D, Himber C, Steinmetz A (2004) Spatial expression of a sunflower SERK gene during induction of somatic embryogenesis and shoot organogenesis. Plant Physiol Biochem 42:35–42PubMedCrossRefPubMedCentralGoogle Scholar
  134. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine rich repeats. Plant Cell 8:735–746PubMedPubMedCentralCrossRefGoogle Scholar
  135. Torres LF, Diniz LEC, do Livramento KG, Freire LL, Paiva LV (2015) Gene expression and morphological characterization of cell suspensions of Coffea Arabica L. cv. Catiguá MG2 in different cultivation stages. Acta Physiol Plant 37:175CrossRefGoogle Scholar
  136. Tucker MR, Araujo AG, Paech NA, Hecht V, Schmidt EDL, Rossell JB, de Vries SC, Koltunow AMG (2003) Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. Plant Cell 15:1524–1537PubMedPubMedCentralCrossRefGoogle Scholar
  137. Vahisalu T, Puzorjova I, Brosche M, Valk E, Lepiku M, Moldau H, Pechter P, Wang YS, Lindgren O, Salojarvi J, Loog M, Kangasjärvi J, Kollist H (2010) Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J 62:442–453PubMedCrossRefPubMedCentralGoogle Scholar
  138. Vilarrasa-Blasi J, Gonzalez-Garcıa MP, Frigola D, Fabregas N, Alexiou KG, Lo´pez-Bigas N, Rivas S, Jauneau A, Lohmann JU, Benfey PN, Ibañes M, Caño-Delgado AI (2014) Regulation of plant stem cell quiescence by a brassinosteroid signaling module. Dev Cell 30:1–12CrossRefGoogle Scholar
  139. Wang H, Mao H (2014) On the origin and evolution of plant brassinosteroid receptor kinases. J Mol Evol 78:118–129PubMedCrossRefPubMedCentralGoogle Scholar
  140. Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15:220–235PubMedCrossRefPubMedCentralGoogle Scholar
  141. Wang ZY, Bai MY, Oh E, Zhu JY (2012) Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46:701–724PubMedCrossRefPubMedCentralGoogle Scholar
  142. Wang Y, Sun S, Zhu W, Jia K, Yang H, Wang X (2013) Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27:681–688PubMedCrossRefPubMedCentralGoogle Scholar
  143. Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, Chang J, Yang W, Chai J (2015) Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525:265–268PubMedCrossRefPubMedCentralGoogle Scholar
  144. Wu W, Wu Y, Gao Y, Li M, Yin H, Lv M, Zhao J, Li J, He K (2015) Somatic embryogenesis receptor-like kinase 5 in the ecotype Landsberg erecta of Arabidopsis is a functional RD LRR-RLK in regulating brassinosteroid signaling and cell death control. Front Plant Sci 6:852PubMedPubMedCentralGoogle Scholar
  145. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22:508–522PubMedPubMedCentralCrossRefGoogle Scholar
  146. Yang C, Zhao T, Yu D, Gai J (2011) Isolation and functional characterization of a SERK gene from soybean (Glycine max (L.) Merr.). Plant Mol Biol Rep 29:334–344CrossRefGoogle Scholar
  147. Zhai L, Xu L, Wang Y, Zhu X, Feng H, Li C, Luo X, Everlyne MM, Liu L (2016) Transcriptional identification and characterization of differentially expressed genes associated with embryogenesis in radish (Raphanus sativus L.). Sci Rep 6:21652PubMedPubMedCentralCrossRefGoogle Scholar
  148. Zhang W, He SY, Assmann SM (2008) The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation. Plant J 56:984–996PubMedPubMedCentralCrossRefGoogle Scholar
  149. Zhang S, Liu X, Lin Y, Xie G, Fu F, Liu H, Wang J, Gao S, Lan H, Rong T (2011) Characterization of a ZmSERK gene and its relationship to somatic embryogenesis in a maize culture. Plant Cell Tissue Organ Cult 105:29–37CrossRefGoogle Scholar
  150. Zhang C, Xu Y, Guo S, Zhu J, Huan Q, Liu H, Wang L, Luo G, Wang X, Chong K (2012) Dynamics of brassinosteroid response modulated by negative regulator LIC in rice. PLoS Genet 8:e1002686PubMedPubMedCentralCrossRefGoogle Scholar
  151. Zhang H, Lin X, Han Z, Wang J, Qu LJ, Chai J (2016) SERK family receptor-like kinases function as co-receptors with PXY for plant vascular development. Mol Plant 9:1406–1414PubMedCrossRefPubMedCentralGoogle Scholar
  152. Zhao DZ, Wang GF, Speal B, Ma H (2002) The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–2031PubMedPubMedCentralCrossRefGoogle Scholar
  153. Zhao B, Lv M, Feng Z, Campbell T, Liscum E, Li J (2016) TWISTED DWARF 1 associates with BRASSINOSTEROID-INSENSITIVE 1 to regulate early events of the brassinosteroid signaling pathway. Mol Plant 9:582–592PubMedCrossRefPubMedCentralGoogle Scholar
  154. Zhu JY, Sae-Seaw J, Wang ZY (2013) Brassinosteroid signalling. Dev 140:1615–1620CrossRefGoogle Scholar
  155. Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16PubMedCrossRefPubMedCentralGoogle Scholar
  156. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760PubMedCrossRefPubMedCentralGoogle Scholar
  157. Zoulias N, Harrison EL, Casson SA, Gray JE (2018) Molecular control of stomatal development. Biochem J 475:441–454PubMedPubMedCentralCrossRefGoogle Scholar
  158. Zuo S, Zhou X, Chen M, Zhang S, Schwessinger B, Ruan D, Yuan C, Wang J, Chen X, Ronald PC (2014) OsSERK1 regulates rice development but not immunity to Xanthomonas oryzae pv. oryzae or Magnaporthe oryzae. J Integr Plant Biol 56:1179–1192PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  1. 1.Research Centre for Plant Growth and Development, School of Life SciencesUniversity of KwaZulu-Natal PietermaritzburgScottsvilleSouth Africa
  2. 2.Department of Biotechnology, Lovely Faculty of Technology and SciencesLovely Professional UniversityPhagwaraIndia

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