Skip to main content
Log in

Abnormal Leaf Morphologies Associated with Primary and Secondary Vein Patterning Defects in Catharanthus roseus: Mid-vein Defect Converts Simple Leaf into Binate Compound Leaf

  • Research Article
  • Published:
Proceedings of the National Academy of Sciences, India Section B: Biological Sciences Aims and scope Submit manuscript

Abstract

Simple petiolated leaves are formed on the wild type plants of apocynaceous medicinal-cum-floricultural species Catharanthus roseus. A C. roseus variant line homozygous for two loss-of-function mutations, an induced leafless inflorescence (lli) mutations and a natural bisected leaf (bil) mutation, was isolated on account of its unique leaf bisection phenotype which was characterized. The lli bil phenotype was highly penetrant but poorly expressed. Only about one-fourth of leaves of lli bil plants were bisected. Leaf bisection was correlated with premature termination of midvein. Degree of bisection varied from a nick at the apex of lamina to formation of two complete leaflets. The notch in 43 % of the bisected leaves bore a pin-like apical adventitious growth. The features of bisected leaves showed that midvein was essential for symmetrical development of smooth lamina spans on its either side; although the development of spans was independent. Several lateral veins emerged from proximal midvein and grew acropetally. Lamina development in the proximal region failed in the absence of local lateral veins. Bisected leaves were also formed as bi-lobed simple leaves, each lobe having its own primary (mid) vein arising from proximally bifurcated midvein. Also formed were completely bisected leaves. In these binately compound leaves, each leaflet had its own petiolule attached to the leaf petiole. The lli bil genotype of C. roseus perhaps provides the only example of a compound leaved variant evolving from a simple leaved species. This phenotype of lli bil leaves supports the suggestion that simple leaf form was ancestral in angiosperms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518

    PubMed  CAS  Google Scholar 

  2. Benkova E, Michniewicz M, Sauer M, Teichmann T, Scifertova D, Jurgens G, Firm J (2003) Local, efflux dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  CAS  Google Scholar 

  3. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Cell Biol 15:1899–1911

    CAS  Google Scholar 

  4. Aida M, Tasaka M (2006) Genetic control of shoot organ boundaries. Curr Opin Plant Biol 9:72–77

    Article  PubMed  CAS  Google Scholar 

  5. Byrne ME, Barley R, Curtis M, Arroya JM, Dunham M, Hudson A, Martienssen RA (2000) ASYMMETRIC LEAVES 1 mediates leaf patterning and stem cell formation in Arabidopsis. Nature 408:967–971

    Article  PubMed  CAS  Google Scholar 

  6. 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

    PubMed  CAS  Google Scholar 

  7. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennet M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260

    Article  PubMed  CAS  Google Scholar 

  8. Ichihashi Y, Kawade K, Usami T, Horiguchi G, Takahashi T, Tsukaya H (2011) Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis. Plant Physiol 157:1151–1162

    Article  PubMed  CAS  Google Scholar 

  9. McConnel JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713

    Article  Google Scholar 

  10. Emery JF, Floyd SK, Alvarej J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANAD1 genes. Curr Biol 13:1768–1774

    Article  PubMed  CAS  Google Scholar 

  11. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic and distinct roles in Arabidopsis development. Plant Cell 17:61–76

    Article  PubMed  CAS  Google Scholar 

  12. Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:3657–3668

    Article  PubMed  CAS  Google Scholar 

  13. Huang W, Pi L, Liang W, Xu B, Wang H, Cai R, Huang H (2006) The proteolytic function of the Arabidopsis 26S proteasome is required for specifying leaf adaxial identity. Plant Cell 18:2479–2492

    Article  PubMed  CAS  Google Scholar 

  14. Yao Y, Ling Q, Wang H, Huang H (2008) Ribosomal proteins promote leaf adaxial identity. Development 135:1325–1334

    Article  PubMed  CAS  Google Scholar 

  15. Pinon V, Etchells JP, Rossignol P, Collier SA, Arroyo JM, Martienssen RA, Byrne ME (2008) Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135:1315–1324

    Article  PubMed  CAS  Google Scholar 

  16. 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 17:2157–2171

    CAS  Google Scholar 

  17. Fu Y, Xu L, Xu B, Yang L, Ling Q, Wang H, Huang H (2007) Genetic interactions between leaf polarity-controlling genes and ASYMMETRIC LEAVES1 and 2 in Arabidopsis leaf patterning. Plant Cell Physiol 48:724–735

    Article  PubMed  CAS  Google Scholar 

  18. Ueno Y, Ishikawa T, Watanabe K, Terakura S, Iwakawa H, Okada K, Machida C, Machida Y (2007) Histone deacetylases and ASYMMETRIC LEAVES2 are involved in the establishment of polarity in leaves of Arabidopsis. Plant Cell 19:445–457

    Article  PubMed  CAS  Google Scholar 

  19. Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128

    PubMed  CAS  Google Scholar 

  20. Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260

    Article  PubMed  CAS  Google Scholar 

  21. Pekker I, Alvarej JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910

    Article  PubMed  CAS  Google Scholar 

  22. Garcia D, Collier S, Byrne M, Martienssen R, Collier S, Byrne M et al (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16:933–938

    Article  PubMed  CAS  Google Scholar 

  23. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554

    Article  PubMed  CAS  Google Scholar 

  24. Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131:2997–3006

    Article  PubMed  CAS  Google Scholar 

  25. Stable MI, Kuehlich J, Staron L, von Amim AG, Golz JF (2009) YABBYs and the transcriptional corepressors LEUNIG and LEUNIG HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21:3105–3118

    Article  Google Scholar 

  26. Sarojam R, Sappl PG, Goldscmidt A, Efroni I, Floyd SK, Eshed Y, Bowman JL (2010) Differentiating Arabidopsis shoots from leaves by combined YABBY activities. Plant Cell 22:2113–2130

    Article  PubMed  CAS  Google Scholar 

  27. Kang J, Dengler N (2002) Cell cycling frequency and expression of the homeobox gene AtHB-8 during leaf vein development in Arabidopsis. Planta 216:212–219

    Article  PubMed  CAS  Google Scholar 

  28. Ilegems M, Douet V, Meylam-Bettex M, Uyttewaal M, Brand L, Bowman JL, Steiger PA (2010) Interplay of auxin, KANADI and class III HD-ZIP III transcription factors in vascular tissue formation. Development 137:975–984

    Article  PubMed  CAS  Google Scholar 

  29. Jun JH, Ha CM, Fletcher JC (2010) BLADE-ON-PETIOLE1 coordinates organ determinacy and axial polarity in Arabidopsis by directly activating ASYMMETRIC LEAVES2. Plant Cell 22:62–76

    Article  PubMed  CAS  Google Scholar 

  30. Townsley BT, Sinha NR (2012) A new development: evolving concepts in leaf ontogeny. Annu Rev Plant Biol 63:535–562

    Article  PubMed  CAS  Google Scholar 

  31. Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027

    Article  PubMed  CAS  Google Scholar 

  32. Wenzel CL, Schuetz M, Yu Q, Mattsson J (2007) Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49:387–398

    Article  PubMed  CAS  Google Scholar 

  33. Dengler N, Kang J (2001) Vascular patterning and leaf shape. Curr Opin Plant Biol 4:50–56

    Article  PubMed  CAS  Google Scholar 

  34. Kang J, Dengler N (2004) Vein Pattern development in adult leaves of Arabidopsis Thaliana. Int J Plant Sci 165:231–242

    Article  Google Scholar 

  35. Donner TJ, Scarpella E (2009) Auxin-transport-dependent leaf vein formation. Botany 87:678–684

    Article  CAS  Google Scholar 

  36. Gardiner J, Donner TJ, Scarpella E (2011) Simultaneous activation of SHR and ATHB8 expression defines switch to preprocambial cell state in Arabidopsis leaf development. Dev Dynam 240:261–270

    Article  CAS  Google Scholar 

  37. Sawchuk MG, Head P, Donner TJ, Scarpella E (2007) Time-lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation. New Phytol 176:560–571

    Article  PubMed  CAS  Google Scholar 

  38. Carland FM, McHale NA (1996) LOP1: a gene involved in auxin transport and vascular patterning in Arabidopsis. Development 122:1811–1819

    PubMed  CAS  Google Scholar 

  39. 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

    Article  PubMed  CAS  Google Scholar 

  40. Carland FM, Berg BL, FitzGerald JN, Jinamornphongs S, Nelson T, Keith B (1999) Genetic regulation of vascular tissue patterning in Arabidopsis. Plant Cell 11:2123–2137

    PubMed  CAS  Google Scholar 

  41. Cnops G, Wang X, Linstead P, Van Montagu M, Van Lijsebettens M, Dolan L (2000) TORNADO 1 and TORNADO 2 are required for the specification of radial and circumferential pattern in the Arabidopsis root. Development 127:3385–3394

    PubMed  CAS  Google Scholar 

  42. Hobbie L, McGovern M, Hurwitz LR, Pierro A, Liu NY, Bandopadhyay A, Estelle M (2000) The axn 6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. Development 127:23–32

    PubMed  CAS  Google Scholar 

  43. Koizumi K, Sugiyama M, Fukuda H (2000) A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. Development 127:3197–3204

    PubMed  CAS  Google Scholar 

  44. Steynen QJ, Schultz EA (2003) The FORKED genes are essential for distal vein meeting in Arabidopsis. Development 130:4695–4708

    Article  PubMed  CAS  Google Scholar 

  45. Petricka JJ, Clay NK, Nelson TM (2008) Vein patterning screens and the defectively organized tributaries mutants in Arabidopsis thaliana. Plant J 56:251–263

    Article  PubMed  CAS  Google Scholar 

  46. Robles P, Fleury D, Candela H, Cnops G, Alonso-Peral MM, Anami S, Falcone A, Caldana C, Willmitzer L, Ponce MR, Van Lijsebettens M, Micol JL (2010) The RON1/FRY1/SAL1 gene is required for leaf morphogenesis and venation patterning in Arabidopsis. Plant Physiol 152:1357–1372

    Article  PubMed  CAS  Google Scholar 

  47. Scarpella E, Francis P, Berleth T (2004) Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131:3445–3455

    Article  PubMed  CAS  Google Scholar 

  48. Luca De, St-Pierre B (2000) The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci 5:168–173

    Article  PubMed  Google Scholar 

  49. El-Sayed M, Verpoorte R (2007) Catharanthus terpenoid indole alkaloids: biosynthesis and regulation. Phytochem Rev 6:277–305

    Article  CAS  Google Scholar 

  50. Chaudhary S, Sharma V, Prasad M, Bhatia S, Tripathi BN, Yadav G, Kumar S (2011) Characterization and genetic linkage mapping of the horticulturally important mutation leafless inflorescence (lli) in periwinkle Catharanthus roseus. Sci Hortic 129:142–153

    Article  CAS  Google Scholar 

  51. Sharma V, Chaudhary S, Srivastava S, Pandey R, Kumar S (2012) Characterization of variation and quantitative trait loci related to terpenoid indole alkaloid yield in a recombinant inbred line mapping population of Catharanthus roseus. J Genet 91:49–69

    Article  PubMed  CAS  Google Scholar 

  52. Kumar S, Rai SP, Rai SK, Singh DV, Srivastava S, Mishra RK (2007) Plant variety of Catharanthus roseus named “lli”. United States Patent

  53. Kulkarni RN, Sreevalli Y, Baskaran K, Kumar S (2001) The mechanism and inheritance of intra flower pollination in self pollinating variant strains of periwinkle. Plant Breed 120:247–250

    Article  Google Scholar 

  54. Kumar S, Chaudhary S, Kumari R, Sharma V, Kumar A (2012) Development of improved horticultural genotypes characterized by novel over-flowering inflorescence trait in periwinkle Catharanthus roseus. Proc Natl Sci Acad India Sect B Biol Sci. doi:10.1007/s40011-012-0048-77

  55. Mishra P, Singh M, Dwivedi S, Kumar S (2000) Descriptores of periwinkle Catharanthus roseus. J Med Aromat Plant Sci 22:268–272

    Google Scholar 

  56. Pandey-Rai S, Luthra R, Kumar S (2003) Salt tolerant mutants in GLYCOPHYTIC SALINITY RESPONSE (GSR) genes in Catharanthus roseus. Theor Appl Genet 106:221–230

    Google Scholar 

  57. Sharma V, Sinha AK, Chaudhary S, Priyadarshini A, Tripathi BN, Kumar S (2012) Genetic analysis of structure and function of stipules in pea Pisum sativum. Proc Ind Natl Sci Acad 78:9–34

    Google Scholar 

  58. Kumar S, Chaudhary S, Sharma V, Kumari R, Mishra RK, Kumar A, Choudhury DR, Jha R, Priyadarshini A, Kumar A (2010) Genetic control of leaf-blade morphogenesis by the INSECATUS gene in Pisum sativum. J Genet 89:201–211

    Article  PubMed  Google Scholar 

  59. Peng J, Chen R (2011) Auxin efflux transporter MtPIN10 regulates compound leaf and flower development in Medicago truncatula. Plant Signal Behav 6:1537–1544

    Article  PubMed  CAS  Google Scholar 

  60. Scarpella E, Barkoulas M, Tsiantis M (2010) Control of leaf and vein development by auxin. Cold Spring Harb Perspect Biol 2:1–17

    Article  Google Scholar 

  61. Macfadyen J (1837) The flora of Jamaica: a description of the plants of that island, arranged according to the natural orders, vol 1. Longman, Orme, Brown, Green, & Longman, London, pp 71–74

    Google Scholar 

  62. Anonymous (2011) Physic nut Jatropha curcus. Weeds of Australia biosecurity Queensland edition. http://keyserver.lucidcentral.org/weeds/data/03030800-0b07-490a-8d04-0605030c0f01/media/Html/Jatropha_curcas.htm

  63. Cambie RC, Brewis A (1997) Anti fertility plants of the Pacific. CSIRO, Collingwood

    Google Scholar 

  64. http://www.fao.org/ag/AGP/AGPC/doc/Gbase/data/pf000094.htm

  65. Don G (1831) A general system of gardening and botany. Gilbert and Rivington, London

    Google Scholar 

  66. Rees A (1820) Encyclopaedia Londinensis, or, Universal dictionary of arts, sciences, and literature, vol 4. Google eBook, London

    Book  Google Scholar 

  67. Efroni I, Eshed Y, Lifschitz E (2010) Morphogenesis of simple and compound leaves: a critical review. Plant Cell 22:1019–1032

    Article  PubMed  CAS  Google Scholar 

  68. Geeta R, Davalos LM, Levy A, Levy A, Bohs L, Lavin M et al (2012) Keeping it simple: flowering plants tend to retain, and revert to, simple leaves. New Phytol 193:481–493

    Article  PubMed  CAS  Google Scholar 

  69. Busch A, Gleissberg S (2003) EcFLO, a FLORICAULA-like gene from Eschscholzia californica is expressed during organogenesis at the vegetative shoot apex. Planta 217:841–848

    Article  PubMed  CAS  Google Scholar 

  70. Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684

    PubMed  CAS  Google Scholar 

  71. 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

    PubMed  CAS  Google Scholar 

  72. Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (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

    Article  PubMed  CAS  Google Scholar 

  73. Zhou C, Labbe H, Sridha S, Wang L, Tian L, Latoszek-Green M, Yang Z, Brown D, Miki B, Wu K (2004) Expression and function of HD2-type histone deacetylases in Arabidopsis development. Plant J 38:715–724

    Article  PubMed  CAS  Google Scholar 

  74. Kojima S, Iwasaki M, Takahashi H, Imai T, Matsumura Y, Fleury D, Van Lijsebettens M, Machida Y, Machida C (2011) Asymmetric leaves2 and Elongator, a histone acetyltransferase complex, mediate the establishment of polarity in leaves of Arabidopsis thaliana. Plant Cell Physiol 52:1259–1273

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Grateful thanks are due to NIPGR for facilities, to Council of Scientific and Industrial Research and Indian National Science Academy for grant of scientist-ship schemes to SK, to SKAIRED for post-MSc fellowship to VS, to RK Mishra and S Chaudhary for their help in scanning of some leaves and to Vinod Kumar for his help in field work. We also gratefully acknowledge useful discussion with Enrico Scarpella by email.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sushil Kumar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kumar, S., Sharma, V. Abnormal Leaf Morphologies Associated with Primary and Secondary Vein Patterning Defects in Catharanthus roseus: Mid-vein Defect Converts Simple Leaf into Binate Compound Leaf. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 83, 241–253 (2013). https://doi.org/10.1007/s40011-012-0090-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40011-012-0090-5

Keywords

Navigation