Skip to main content
SpringerLink
Log in

Pulvinus or not pulvinus, that is the question: anatomical features of the petiole in the Citrus family (Rutaceae, Sapindales)

  • Structural Botany - Original Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Several Rutaceae species have petioles with a swollen apical and/or a basal region and a thinner middle portion. These swollen petiolar regions are morphologically similar to pulvini but are recognized by an array of other nomenclatures. We hypothesized that the swollen regions in Rutaceae petioles present anatomical features in keeping with pulvini. We accessed the anatomical features of the petioles in 11 species of Rutaceae belonging to four subfamilies, comparing the swollen and middle petiolar regions. Samples were cross-sectioned using razor blade and stained with Astra Blue and Safranin. Other samples were embedded in methacrylate resin; cross and longitudinal sections were obtained using a rotating microtome and stained with toluidine Blue. Semi-permanent and permanent slides were analyzed using a light microscope. Cortex is significantly wider than in the middle petiolar portion in the swollen petiolar regions. Collenchyma and parenchyma are present in the cortex in all the petiolar regions; sclerenchyma cells are more commonly observed in the middle petiolar region. Secondary growth occurs in all the petiolar regions, but it is more well established in the middle portion of petioles. Septate fibers with non-lignified walls and gelatinous fibers occur externally to the phloem in the swollen, but not in the middle petiolar regions—such petiolar region exhibits only perivascular fibers with completely lignified walls. Articulations were observed only in Citrus × limonia. Several anatomical features observed in the swollen petiolar regions in Rutaceae are similar to those described to pulvini in other Angiosperms and can be associated with lower rigidity of this region. However, considering the lack of records on the occurrence of leaf movement in this family so far, we suggest the use of “pulvinus-like thickenings” in Rutaceae petioles, and the terms “distal pulvinus-like thickening” and “proximal pulvinus-like thickenings” for the thickened regions near the apex and base of the leaf, respectively. Ultrastructural and leaf movement studies in Rutaceae are needed to clarify the nature and of the thickened petiole regions in the family.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Appelhans MS, Bayly MJ, Heslewood MM, Groppo M, Verboom A, Forster PI, Kallunki JA, Duretto MF (2021) A new subfamily classification of the Citrus family (Rutaceae) based on six nuclear and plastid markers. Taxon. https://doi.org/10.1002/tax.12543

    Article  Google Scholar 

  • Arioli T, Voltolini CH, Santos M (2008) Morfoanatomia foliar da reófita Raulinoa echinata R.S. Cowan—Rutaceae. Acta Bot Bras 22:723–732

    Article  Google Scholar 

  • Bell AD, Bryan A (2008) Plant form: an illustrated guide to flowering plant morphology. Timber Press, Portland, 431p

    Google Scholar 

  • Bruniera CP, Silva CID, Groppo M (2011) A new species of Almeidea (Galipeinae, Galipeeae, Rutaceae) from Eastern Brazil. Brittonia 63:281–285

    Article  Google Scholar 

  • Bruniera CP, Kallunki JA, Silva IM, Silva CID, Groppo M (2021) A revision of Conchocarpus with pantocolporate pollen grains: the Almeidea Group (Galipeinae, Rutaceae). Syst Bot 46:375–388

    Article  Google Scholar 

  • Bruniera CP, Groppo M, Kallunki JA (2015) Almeidea A.St-Hil. belongs to Conchocarpus J.C. Mikan (Galipeinae, Rutaceae): evidence from morphological and molecular data, with a first analysis of subtribe Galipeinae. PLoS One 10: e0125650. https://doi.org/10.1371/journal.pone.0125650.

  • Bukatsch F (1972) Bemerkungen zur Doppelfarbung: Astrablau-Safranin. Mikrokosmos 61:255

    Google Scholar 

  • Caldas LSL, Lüttge U, Franco AC, Haridasan M (1997) Leaf heliotropism in Pterodon pubescens, a woody legume from the brazilian cerrado. Rev Bras Fisiol Veg 9:1–7

    Google Scholar 

  • Campbell NA, Garber RC (1980) Vacuolar reorganization in motor cells of Albizzia during leaf movement. Planta 148:251–255

    Article  CAS  PubMed  Google Scholar 

  • Campbell NA, Thomson WW (1977) Multivacuolate motor cells in Mimosa pudica L. Ann Bot 41:1361–1362

    Article  Google Scholar 

  • Campbell NA, Stika KM, Morrison GH (1979) Calcium and potassium in the motor organ of the sensitive plant: localization by ion microscope. Science 204:185–187

    Article  CAS  PubMed  Google Scholar 

  • Chang S-C, Cho MH, Kang BG, Kaufman PB (2001) Changes in starch content in oat (Avena sativa) shoot pulvini during the gravitropic response. J Exp Bot 52:1029–1040

    Article  CAS  PubMed  Google Scholar 

  • Cruz R, Duarte M, Pirani JR, Melo-De-Pinna GFA (2015) Development of leaves and shoot apex protection in Metrodorea and related species (Rutaceae). Bot J Linn Soc 178: 267–282

    Article  Google Scholar 

  • Cruz R , Duarte M, Pirani JR, Melo-de-Pinna GFA (2017) Phylogenetic analysis and evolution of morphological characters in Metrodorea and related species in Rutoideae (Rutaceae). Plant Syst Evol 303: 927–943

    Article  Google Scholar 

  • Dayanandan P, Herbard FV, Kaufman PB (1977) Cell elongation in the grass pulvinus in response to geotropic stimulation and auxin application. Planta 132:245–252

    Google Scholar 

  • Fleurat-Lessard P (1981) Ultrastructural features of the starch sheath cells of the primary pulvinus after gravistimulation of the sensitive plant (Mimosa pudica L.). Protoplasma 105:177–184

    Article  Google Scholar 

  • Fleurat-Lessard P (1988) Structural and ultrastructural features of cortical cells in motor organs of sensitive plants. Biol Rev 63:1–22

    Article  Google Scholar 

  • Fleurat-Lessard P, Bonnemain J-L (1978) Structural and ultrastrucutral characteristics of the vascular apparatus of the sensitive plant (Mimosa pudica L.). Protoplasma 94:127–143

    Article  Google Scholar 

  • Fleurat-Lessard P, Millet B (1984) Ultrastructural features of cortical parenchyma cells (“motor cells”) instamen of Berberis canadensis Mill. and terciary pulvini of Mimosa pudica L. J Exp Bot 35:1332–1341

    Article  Google Scholar 

  • Fleurat-Lessard P, Roblin G (1982) Comparative histocitology of the petiole and the main pulvinus in Mimosa pudica L. Ann Bot 50:83–92

    Article  Google Scholar 

  • Grignon N, Touraine B, Grignon C (1992) Internal phloem in the pulvinus of soybean plants. Am J Bot 50:83–92

    Google Scholar 

  • Groppo M, Kallunki JA, Pirani JR, Antonelli A (2012) Chilean Pitavia more close related to Oceania and Old World Rutaceae than to Neotropical groups: evidence from two cpDNA non-coding regions, with a new subfamilial classification of the family. Phytokeys 19:9–29

    Article  Google Scholar 

  • Groppo M, Lemos, LJC, Ferreira, PL, Ferreira C,Bruniera CP, Castro, NM, Pirani JR, Kallunki JA (2021) A tree nymph of the Brazilian Atlantic Forest: Dryades (Galipeinae, Rutaceae), a new neotropical genus segregated from Conchocarpus. Mol Phylogen Evol 154:106971. https://doi.org/10.1016/j.ympev.2020.106971

  • Groppo M, Afonso LF, Pirani JR (2021). A review of systematics studies in Rutaceae (Sapindales), with emphasis on American groups. Braz J Bot (in press)

  • Hagihara T, Toyota M (2020) Mechanical signaling in the sensitive plant Mimosa pudica L. plants 9:587. https://doi.org/10.3390/plants9050587

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometr J 50:346–363

    Article  Google Scholar 

  • Howard RA (1979) The petiole. In: Metcalfe CR, Chalk L (Eds) Anatomy of the dicotyledons—systematics anatomy of leaf, and stem, with a brief history of the subject, 2nd ed. Clarendon Press, Oxford, pp 88–96

  • Inyama CN, Vun O, Mbagwu FN, Duru CM (2015) Comparative morphology of the leaf epidermis in six Citrus species and its biosystematic importance. Med Aromat Plant. https://doi.org/10.4172/2167-0412.1000194

    Article  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. Mc Graw Hill, New York

    Google Scholar 

  • Kallunki JA, Pirani JR (1998) Synopses of Angostura Roem. & Schult. and Conchocarpus J.C.Mikan. Kew Bull 53:257–334

    Article  Google Scholar 

  • Knapp S (2009) Taxonomy as a team sport. In: Wheeler QD (ed) The new taxonomy. CRC Press, New York, pp 33–50

    Google Scholar 

  • Kozak M, Piepho H-P (2018) What’s normal anyway? Residual plots are more telling than significance tests when checking ANOVA assumptions. J Agron Cr Sci 204:86–98

    Article  Google Scholar 

  • Kubitzki K, Kallunki JA, Duretto M, Wilson PG (2011) Rutaceae. In: Kubitski K (ed) The families and genera of vascular plant. Flowering plants. Eudicots: Sapindales, Cucurbitales, Myrtaceae. Springer, Berlin, pp 276–356

  • Lepš ŠJ, Šmilauer P (2020) Biostatistics with R: an introductory guide for field biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Leroux O (2012) Collenchyma: a versatile mechanical tissue with dynamic cell walls. Ann Bot 110:1083–1098

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopes LTA, Paula JR, Tresvenzol LMF, Bara MTF, Sá S, Ferri PH, Fiuza TS (2013) Composição química e atividade antimicrobiana do óleo essencial e anatomia foliar e caulinar de Citrus limettioides Tanaka (Rutaceae). Rev Ciênc Farm Bas Apl 34:503–511

    Google Scholar 

  • Machado SR, Rodrigues TM (2004) Anatomia e ultra-estrutura do pulvino primário de Pterodon pubescens Benth. (Fabaceae-Faboideae). Rev Bras Bot 27:135–147

    Article  Google Scholar 

  • Morse MJ, Satter RL (1979) Relationship between motor cell ultrastructure and leaf movements in Samanea saman. Physiol Plant 46:338–346

    Article  Google Scholar 

  • Moysset L, Simón E (1991) Secondary pulvinus of Robinia pseudoacacia (Leguminosae): structural and ultrastructural features. Am J Bot 78:1467–1486

    Article  Google Scholar 

  • Moysset L, Llambrich E, Simon E (2019) Calcium changes in Robinia pseudoacacia pulvinar motor cells during nyctinastic closure mediated by phytochromes. Protoplasma 256:615–629

    Article  CAS  PubMed  Google Scholar 

  • Muntoreanu TG, Cruz RS, Melo-de-Pinna GF (2011) Comparative leaf anatomy and morphology of some neotropical Rutaceae: Pilocarpus Vahl and related genera. Plant Syst Evol 296:87–99

    Article  Google Scholar 

  • Muntoreanu TG (2008) Descrição e mapeamento de caracteres morfo-anatômicos foliares em Pilocarpus Vahl (Rutaceae) e gêneros relacionados. Dissertation, Universidade de São Paulo, São Paulo

  • O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue. Protoplasma 59:368–373

  • Ogundare CS, Saheed SA (2012) Foliar epidermal characters and petiole anatomy of four species of Citrus l. (Rutaceae) from South-Western Nigeria. Bangladesh J Plant Taxon 19:25–31

    Article  Google Scholar 

  • Parnell J, Rich T, McVeigh A, Lim A, Quigley S, Morris D, Wong Z (2013) The effect of preservation methods on plant morphology. Taxon 62:1259–1265

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) nlme: Linear and nonlinear mixed effects models. R package version 3.1–128. http://CRAN.R-project.org/package=nlme. Accessed 09 September 2021

  • Pirani JR (1999) Estudos taxonômicos em Rutaceae: revisão de Helietta e Balfourodendron (Pteleinae), análise cladística de Pteleinae, sinopse de Rutaceae no Brasil. Universidade de São Paulo, São Paulo, Thesis

    Google Scholar 

  • Pirani JR, Groppo M, Kallunki JA (2012) Two new species and a new combination in Conchocarpus (Rutaceae, Galipeinae) from eastern Brazil. Kew Bull 66:521–527

    Article  Google Scholar 

  • Pirani JR (2002) Rutaceae. In: Wanderley MGL, Shepherd GJ, Giulietti AM (eds) Flora Fanerogâmica do Estado de São Paulo. Hucitec, São Paulo, pp 281–308.

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 09 September 2021

  • Roblin G, Fleurat-Lessard P, Bonmort J (1989) Effects of compounds affecting calcium channels on phytochrome- and blue pigment-mediated pulvinar movements of Cassia fasciculata. Plant Physiol 90:697–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues TM, Machado SR (2004) Anatomia comparada do pulvino, pecíolo e raque de Pterodon pubescens Benth. (Fabaceae-Faboideae). Acta Bot Bras 18:381–390

    Article  Google Scholar 

  • Rodrigues TM, Machado SR (2006) Anatomia comparada do pulvino primário de leguminosas com diferentes velocidades de movimento foliar. Rev Bras Bot 29:709–720

    Article  Google Scholar 

  • Rodrigues TM, Machado SR (2007) The pulvinus endodermal cells and their relations to leaf movement in legumes of the Brazilian Cerrado. Plant Biol 9:469–477

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues TM, Machado S (2008) Pulvinus functional traits in relation to leaf movements: a light and transmission electron microscopy study of the vascular system. Micron 39:7–16

    Article  PubMed  Google Scholar 

  • Santo AE, Pugialli HRLP (1999) Estudo da Plasticidade Anatômica Foliar de Stromanthe thalia (Vell.) J.M.A. Braga (Marantaceae) em Dois Ambientes de Mata Atlântica. Rodriguésia 50:109–124

    Article  Google Scholar 

  • Satter RL, Galston AW (1981) Mechanisms of control of leaf movements. Ann Rev Plant Physiol 32:83–110

    Article  CAS  Google Scholar 

  • Satter RL, Garber RC, Khairallah L, Cheng Y-S (1982) Elemental analysis of freeze-dried thin sections of Samanea motor organs: barriers to ion diffusion through the apoplast. J Cell Biol 95:893–902

    Article  CAS  PubMed  Google Scholar 

  • Schrempf M, Satter RL, Galston AW (1976) Potassium-linked chloride fluxes during rhythmic leaf movement of Albizzia julibrissin. Plant Physiol 58:190–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Souza VC, Lorenzi H (2008) Botânica sistemática: guia ilustrado para identificação das famílias de fanerógamas nativas e exóticas no Brasil, baseado em APG II. Instituto Plantarum, São Paulo

  • Swingle WT, Reece PC (1967) The botany of citrus and its wild relatives. In: Reuther W, Webber HJ, Batchelor LD (eds) The Citrus industry. University of California, Riverside, pp 190–430

    Google Scholar 

  • Thiers B (2016) Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/ih/

  • Tomaszewski D, Górzkowska A (2016) Is shape of a fresh and dried leaf the same? PLoS ONE 11:e0153071. https://doi.org/10.1371/journal.pone.0153071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toriyama H (1953) Observational and experimental studies of sensitive plants I: the structure of parenchymatous cells of pulvinus. Cytology 18:283–292

    Article  Google Scholar 

  • Toriyama H (1954) Observational and experimental studies of sensitive plants. II. On the changes in motor cells of diurnal and nocturnal condition. Cytology 19:29–40

    Article  Google Scholar 

  • Toriyama H (1955) Observational and experimental studies of sensitive plants. V. The development of the tannin vacuole in the motor cell of the pulvinus. Bot Mag 68:203–208

    Article  Google Scholar 

  • Toriyama H (1957) Observational and experimental studies of sensitive plants. VII. The migration of colloidal substance in the primary pulvinus. Cytology 22:184–192

    Article  Google Scholar 

  • Toriyama H (1967) A comparison of the Mimosa motor cells before and after stimulation. Proc Jpn Acad 43:541–546

    Article  Google Scholar 

  • Toriyama H, Jaffe MJ (1972) Migration of calcium and its role in the regulation of seismonasty in the motor cell of Mimosa pudica L. Plant Physiol 49:72–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toriyama H, Komada Y (1971) The recovery process of the tannin vacuole in the motor cell of Mimosa pudica L. Cytology 36:690–697

    Article  CAS  Google Scholar 

  • Toriyama H, Satô S (1968) Electron microscopic observations of the motor cells of Mimosa pudica L. I. A comparison of the motor cells before and after stimulation. Proc Jpn Acad 44:702–706

    Article  Google Scholar 

  • Uehlein N, Kaldenhoff R (2008) Aquaporins and plant leaf movements. Ann Bot 101:1–4

    Article  CAS  PubMed  Google Scholar 

  • Vun O, Mbagwu FN, Inyama CN, Ukpai KU (2015) Stematic characterization of six Citrus Species using petiole anatomy. Med Aromat Plant. https://doi.org/10.4172/2167-0412.S1-005

    Article  Google Scholar 

  • Yamashiro S, Kameyama K, Kanzawa N, Tamiya T, Mabuchi I, Tsuchiya T (2001) The gelsolin/fragmin family protein identified in the higher plant Mimosa pudica. J Biochem 130:243–249

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq—for the research productivity fellowship to MG (grant #311969/2019-4) and to TMR (Grant #303981/2018-0). MG also thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for financial support (Process #2016/06260-2). This study was funded in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil, CAPES (Finance Code 001). CF thanks her Doctoral Thesis Committee members for discussion and their suggestions in an earlier version of the text, as well as two anonymous reviewers. Fernando Farache is acknowledge for his help in the figures and statistical analysis. We also thank Diego Demarco and José Rubens Pirani for their technical guidance and support.

Author information

Authors and Affiliations

  1. Departamento de Biologia, FFCLRP, Universidade de São Paulo, Av. Bandeirantes 3900, Ribeirão Preto, SP, 14040-901, Brazil

    Carolina Ferreira & Milton Groppo

  2. Instituto de Biologia, Universidade Federal de Uberlândia, Campus Umuarama, Av. Pará 1.720, Uberlândia, MG, 38400-902, Brazil

    Neuza Maria Castro

  3. Departamento de Bioestatística, Biologia Vegetal, Parasitologia e Zoologia, Instituto de Biociências, Universidade Estadual Paulista UNESP, Rua Prof. Dr. Antônio Celso Wagner Zanin s/n, Botucatu, SP, 18618-970, Brazil

    Tatiane Maria Rodrigues & Diana Pacheco Seixas

Authors
  1. Carolina Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neuza Maria Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatiane Maria Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Diana Pacheco Seixas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Milton Groppo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CF collected data on anatomy, performed analyses, and wrote the paper. TMR collected data on anatomy, performed analyses, and wrote the paper. DPS collected data on anatomy, performed analyses, and wrote the paper. NMC collected data on foliar anatomy and wrote the paper. MG provided funds and wrote the paper.

Corresponding author

Correspondence to Milton Groppo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ferreira, C., Castro, N.M., Rodrigues, T.M. et al. Pulvinus or not pulvinus, that is the question: anatomical features of the petiole in the Citrus family (Rutaceae, Sapindales). Braz. J. Bot 45, 485–496 (2022). https://doi.org/10.1007/s40415-021-00782-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-021-00782-0

Keywords

Search

Navigation