Abstract
In this review, our analyses of the metabolic routes of limonoids and quassinoids—with respect to their occurrence in the families Rutaceae, Meliaceae, and Simaroubaceae—suggest a disjunction between the Simaroubaceae (characterized by quassinoids) and the Rutaceae and Meliaceae (distinguished by limonoids). However, even with the latter two families, clear-cut chemical differences could be discerned. Meliaceae exploit different biogenetic pathways, which lead to more diverse limonoids than in Rutaceae. The complex limonoids and prenylated chromones isolated from Spathelia, Sohnreyia, Dictyoloma, Harrisonia, Cneorum, and Cedrelopsis provided firm support for including them into the Cneoroideae. Ptaeroxylon produces several types of chromones, justifying to include it near the allied taxa, also into Cneoroideae. However, considering the complex limonoids found in Flindersia and Hortia, their connections to the Rutoideae subfamily were thus rather difficult to envisage; they suggest a closer relationship with the Cneoroideae genera. Until recently, there was no chemical evidence to support the placement of Picramnia into Simaroubaceae or near the allied taxa Rutaceae and Meliaceae. However, our investigations revealed several nortriterpenes involving expansion of the A-ring to a 4,4-dimethyl-tetrahydro-2H-furo[1,10]pyran-3(6H)-one as in limonin-type limonoids, whose derivatives have been isolated from Rutaceae genera. In addition, liquid chromatography-tandem mass spectrometry-(MS/MS)-based molecular networking showed profiling of quassinoids from P. glazioviana. These data convincingly point to affinities between Picramnia species and Cneoroideae genera, suggesting Picramniaceae is sister to Rutaceae, Simaroubaceae, and Meliaceae.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alves IABS, Miranda HM, Soares LAL, Randau KP (2014) Simaroubaceae family: botany, chemical composition and biological activities. Braz J Pharmacog 24:481–550. https://doi.org/10.1016/j.bjp.2014.07.021
Appelhans MS, Smets E, Razafimandimbison SG, Haevermans T, van Marle EJ, Couloux A, Rabarison H, Randrianarivelojosia M, Keßler PJA (2011) Phylogeny, evolutionary trends and classification of the Spathelia-Ptaeroxylon clade: morphological and molecular insights. Ann Bot 107:1259–1277. https://doi.org/10.1093/aob/mcr076
Balderrama L, Braca A, Garcia E, Melgarejo M, Pizza C, De Tommasi N (2001) Triterpenes and anthraquinones from Picramnia sellowii Planchon in Hook (Simaroubaceae). Biochem Syst Ecol 29:331–333
Breen GW, Picker K, Raston CL, Skelton BW, Taylor WC, White AH (1984) Chemical constituents of the Flindersia. XXIII Determination of the structure of flindercarpin-2 as methyl (S)-(acetoxy){[30S-(3a,3aa,4a,5b,6a,6aa,7a,10aa,11aa)]-50,60-diacetoxy-70-(furan-300-yl)-20,20,3a0,6a0,11a0-pentamethyl-120-methylene-90-oxo-20,30,3a0,40,50,60,6a0,90,100,11a0-decahydro-70H-40,10a0-methano-10a0H-furo[2,3-b]pyrano-[3,4-g]oxocin-30-yl}acetate. Aust J Chem 37:1461–1471. https://doi.org/10.1071/CH9841461
Byrne LT, Tri MV, Phuong NM, Sargent MV, Skelton BW, White AH (1991) Perforatin: a novel tetranortriterpenoid from Harrisonia perforate. Aust J Chem 44:165–169. https://doi.org/10.1071/CH9910165
Carvalho LE, Lima MP, Máximo AC, Pereira ECS, Moreira WAS, Ferreira AG, Véras SM, Souza MG (2012) Estudo em raiz e ráquis foliar de Spathelia excelsa: fitoquímica e atividade frente ao fungo Moniliophthora perniciosa associado ao cupuaçuzeiro (Theobroma grandiflorum). Quim Nova 35:2237–2240
Chapman JL (1987) Sporne's advancement index revisited. New Phytol 106:319–332. http://www.jstor.org/stable/2434863
Chase MW, Morton CM, Kallunki JA (1999) Phylogenetic relationships of Rutaceae: a cladistic analysis of the subfamilies using evidence from rbcL and atpB sequence variation. Am J Bot 86:1191–1199. https://doi.org/10.2307/2656983
Choodej S, Sommit D, Pudhom K (2013) Rearranged limonoids and chromones from Harrisonia perforata and their anti-inflammatory activity. Bioorg Med Chem Lett 23:3896–3900. https://doi.org/10.1016/j.bmcl.2013.04.064
Clayton JW (2011) Simaroubaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Springer, Berlin
Cole TCH, Groppo M (2020) Filogenia das Rutaceae. https://www.researchgate.net/publication/324834989
Dalisay DS, Molinski TF (2009) NMR quantitation of natural products at the nanomole-scale. J Nat Prod 72:739–744
Diaz F, Chai HB, Mi Q, Su BN, Vigo JS, Graham JG, Cabieses F, Farnsworth NR, Cordell GA, Pezzuto JM, Swanson SM, Kinghorn AD (2004) Anthrone and oxanthrone C-glycosides from Picramnia latifolia collected in Peru. J Nat Prod 67:352–356. https://doi.org/10.1021/np030479j
Engler A (1896) Rutaceae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien, Teil III, Abt. 4–5. Engelmann, Leipzig, pp 95–201
Engler A (1931) Rutaceae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien. Leipizig, Wilhelm Engelmann, pp 187–359
Epe B, Mondon A (1979) Zur Kenntnis Der Bitterstoffe Aus Cneoraceen, XII. Tetrahedron Lett 22:2015–2018
Fang X, Di YT, Hao XJ (2011) The advances in the limonoid Chemistry of the Meliaceae family. Curr Org Chem 15:1363–1391. https://doi.org/10.2174/138527211795378254
Fang X, Di YT, Zhang Y, Xu ZP, Lu Y, Chen QQ, Zheng QT, Hao XJ (2015) Unprecedented quassinoids with promising biological activity from Harrisonia perforata. Angew Chem Int 54:1–5. https://doi.org/10.1002/anie.201412126
Fernando ES, Quinn CJ (1995) Picramniaceae, a new family, and a recircumscription of Simaroubaceae. Taxon 44:177–181. https://doi.org/10.2307/1222440
Fernando ES, Gadek PA, Crayn DM, Quinn CJ (1993) Rosid affinities of Surianaceae: molecular evidence. Mol Phylogenet Evol 2:344–350. https://doi.org/10.1006/mpev.1993.1034
Fernando ES, Gadek PA, Quinn CJ (1995) Simaroubaceae, an artificial construct: evidence from rbcL sequence variation. Am J Bot 82:92–103. https://doi.org/10.2307/2445791
Gadek PA, Fernando ES, Quinn CJ, Hoot SB, Terrazas T, Sheahan MC, Chase MW (1996) Sapindales: molecular delimitation and infraordinal groups. Am J Bot 83:802–811. https://doi.org/10.2307/2445857
Gimenes L, Batista JM Jr, dos Santos Jr FM, Souza MS, Luna-Dulcey L, Ellena J, Cominetti MR, da Silva MFGF, Viera PC, Fernandes JB, Staerk D (2019) Picraviane A and B: nortriterpenes with limonoid-like skeletons containing a heptanolide E-ring system from Picramnia glazioviana. Phytochemistry 163:38–45
Gimenes L, Luna-Dulcey L, Batista-Jr JM, Santos-Jr FM, Popolin CP, Cominetti MR, Fernandes JB, Staerk D (2020) Structure elucidation and absolute configuration determination of nortriterpenoids from Picramnia glazioviana. J Nat Prod 83:1859–1875
Gray AI (1983) Coumarins and chromones in the Rutales. In: Waterman PG, Grundon MF (eds) Chemistry and chemical taxonomy of the Rutales. Academic Press, London
Groppo M, Pirani JR, Salatino MLF, Blanco SR, Kallunki JA (2008) Phylogeny of Rutaceae based on two noncoding regions from cpDNA. Am J Bot 95:985–1005. https://doi.org/10.3732/ajb.2007313
Harms H (1931) In: Dienatürlichen Pflanzenfamilien - Nachtrage zu Band 19a. Engler A, Harms H (eds). Verlag von Wilhelm Engelmann, Leipzig, pp 457
Hegnauer R (1983) Chemical characteres and the classification of the Rutales. In: Waterman PG, Grundon MF (eds) Chemistry and chemical taxonomy of the Rutales. Academic Press, London, UK, pp 401–440
Hernández-Mendel MDR, Garcia-Salmones I, Santillan R, Trigos A (1998) An anthrone from Picramnia antidesma. Phytochemistry 49:2599–2601. https://doi.org/10.1016/S0031-9422(98)00383-5
Hernández-Mendel MDR, Ramirez-Corzas CO, Riviera-Dominguez MN, Ramirez-Mendez J, Santillan R, Rojas-Lima S (1999) Diastereomeric C-glycosyloxanthones from Picramnia antidesma. Phytochemistry 50:1379–1383. https://doi.org/10.1016/S0031-9422(98)00354-9
Jacobs H (2003) Comparative phytochemistry of Picramnia and Alvaradoa, genera of the newly established family Picramniaceae. Biochem Syst Ecol 31:773–783. https://doi.org/10.1016/S0305-1978(02)00268-5
Jacobs H, Ramdayal F (1986) Guyanin, a novel tetranortriterpenoid. Structure elucidation by 2D NMR spectroscopy. Tetrahedron Lett 27:1453–1456. https://doi.org/10.1016/S0040-4039(00)84283-5
Khuong-Huu Q, Chiaroni A, Riche C, Nguyen-Ngoc H, Nguyen-Viet K, Khoung-Huu F (2000) New rearranged limonoids from Harrisonia perforata. J Nat Prod 63:1015–1018. https://doi.org/10.1021/np990598s
Khuong-Huu Q, Chiaroni A, Riche C, Nguyen-Ngoc H, Nguyen-Viet K, Khuong-Huu F (2001) New rearranged limonoids from Harrisonia perforata III. J Nat Prod 64:634–637. https://doi.org/10.1021/np000471z
Krause K (1914) Notizblatt Des Koniglichen Botanischen Gartens Und Museums Zu Berlin 55:143
Kubitzki K, Kallunki JA, Duretto M, Wilson PW (2011) Rutaceae. In: Kubitzki K (ed) The families and genera of vascular plants: flowering plants. Eudicots: Sapindales, Cucurbitales, Myrtaceae. Springer, Berlin
Kubitzki K (ed) (2011) The families and genera of vascular plants: Flowering plants. Eudicots, Sapindales, Cucurbitales, Myrtaceae. Springer, Berlin
Logacheva M, Shipunov A (2017) Phylogenomic analysis of Picramnia, Alvaradoa, and Leitneria supports the independent Picramniales. J Syst Evol 55:171–176. https://doi.org/10.1111/jse.12246
Mabberley DJ (2011) Meliaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Springer, Berlin
Martinez ML, von Poser G, Henriques A, Gattuso M, Rossini C (2013) Simaroubaceae and Picramniaceae as potential sources of botanical pesticides. Ind Crops Prod 44:600–602. https://doi.org/10.1016/j.indcrop.2012.09.015
Mi Q, Lantvit D, Reyes-Lim E, Chai H, Phifer SS, Wani MC, Wall ME, Tan GT, Cordell GA, Farnsworth NR, Kinghorn AD, Pezzuto JM (2005) Apoptotic anticancer effect of alvaradoin E isolated from Alvaradoa haitiensis. Anticancer Res 25:779–787
Moreira ASN, Mathias L, Braz-Filho R, Schripsema J, Vieira I (2002) Two new diprenylated coumarins from Flindersia brayleyana. Nat Prod Lett 16:291–295. https://doi.org/10.1080/10575630290020668
Morton CM, Telmer C (2014) New subfamily classification for the Rutaceae. Ann Mo Bot Gard 99:620–641. https://doi.org/10.3417/2010034
Muellner AN, Samuel R, Johnson SA, Cheek M, Pennington TD, Chase MW (2003) Molecular phylogenetics of Meliaceae based on nuclear and plastid DNA sequences. Am J Bot 90:471–480. https://doi.org/10.3732/ajb.90.3.471
Muellner AN, Savolainen V, Samuel R, Chase MW (2006) The mahogany family “out-of-Africa”: divergence time estimation, global biogeographic patterns inferred from plastid rbcL DNA sequences, extant, and fossil distribution of diversity. Mol Phylogenet Evol 40:236–250. https://doi.org/10.1016/j.ympev.2006.03.001
Muellner AN, Samuel R, Chase MW, Coleman A, Stuessy TF (2008) An evaluation of the tribes and of generic relationships in Melioideae (Meliaceae) based on nuclear ITS ribosomal DNA. Taxon 57:98–108. https://doi.org/10.2307/25065951
Mulholland DA, Mahomed H, Randrianarivelojosia M, Lavaud C, Massiot G, Nuzillard J (1999) Limonoid derivatives from Cedrelopsis grevei. Tetrahedron 55:11547–11552. https://doi.org/10.1016/S0040-4020(99)00653-5
Mulholland DA, Schwikkard SF, Sandor P, Nuzillard JM (2000) Delevoyin C, a tetranortriterpenoid from Entandrophragma delevoyi. Phytochemistry 53:465–468. https://doi.org/10.1016/S0031-9422(99)00546-4
Mulholland DA, Naidoo D, Randrianarivelojosia M, Cheplogoi PK, Coombes PH (2003) Secondary metabolites from Cedrelopsis grevei (Ptaeroxylaceae). Phytochemistry 64:631–635. https://doi.org/10.1016/s0031-9422(03)00342-x
Paritala V, Chiruvella KK, Thammineni C, Ghanta RG, Mohammed A (2015) Phytochemicals and antimicrobial potentials of mahogany family. Braz J Pharmacog 25:61–83. https://doi.org/10.1016/j.bjp.2014.11.009
Pennington TD, Styles BT (1975) A generic monograph of the Meliaceae. Blumea 22:419–540. https://doi.org/10.2307/4110009
Phifer SS, Lee D, Seo EK, Kim NC, Graf TN, Kroll DJ, Navarro HA, Izydore RA, Jimenez F, García R, Rose WC, Fairchild CR, Wild R, Soejarto DD, Farnsworth NR, Kinghorn AD, Oberlies NH, Wall ME, Wani MC (2007) Alvaradoins E-N, antitumor and cytotoxic anthracenone C-glycosides from the leaves of Alvaradoa haitiensis. J Nat Prod 70:954–961. https://doi.org/10.1021/np070005a
Plunkett GM, Pimenov MG, Reduron JP, Kljuykov EV, van Wyk BE, Ostroumova TA, Henwood MJ, Tilney PM, Spalik K, Watson MF, Lee BY, Pu FD, Webb CJ, Hart JM, Mitchell AD, Muckensturm B (2018) Apiaceae. In: Bittrich V (ed) Kadereit J. Flowering plants. Eudicots. The families and genera of vascular plants, Springer, Cham
Popinigis I, Moreira EA, Nakashima T, Krambeck R, Miguel OG (1980) Contribuicao ao estudo farmacognostico de picramnia parvifolia engler. Simaroubageae. Trib Farm 48:24–43
Quintal-Novelo C, Torres-Tapia LW, Moo-Puc R, Peraza-Sanchez SR (2015) Cytotoxic constituents from the stem bark of Alvaradoa amorphoides. J Mex Chem Soc 59:211–214
Rajab MS, Rugutt JK, Fronczek FR, Fischer NH (1997) Structural revision of harrisonin and 12 β-acetoxyharrisonin, two limonoids from Harrisonia abyssinica. J Nat Prod 60:822–825. https://doi.org/10.1021/np970201p
Rajaba MS, Fronczekb FR, Mulhollandc DA, Rugutt JK (1999) 11β,12β-Diacetoxyharrisonin, a tetranortriterpenoid from Harrisonia abyssinica. Phytochemistry 52:127–133. https://doi.org/10.1016/S0031-9422(99)00096-5
Rodrígues-Gamboa T, Victor SR, Fernandes JB, Rodrigues-Fo E, Silva MFGF, Vieira PC, Pagnocca FC, Bueno OC, Hebling MJA, Castro O (2000) Anthrone and oxanthrone C, O-diglycosides from Picramnia teapensis. Phytochemistry 55:837–841. https://doi.org/10.1016/s0031-9422(00)00323-x
Rodriguez-Gamboa T, Fernandes JB, Rodrigues-Fo ER, Silva MFDG, Vieira PC, Castro O (1999) Two anthrones and one oxanthrone from Picramnia teapensis. Phytochemistry 51:583–586. https://doi.org/10.1016/S0031-9422(99)00023-0
Rodriguez-Gamboa T, Fernandes JB, Rodrigues-Fo E, Silva MF, Vieira PC, Barrios CM, Castro-Castillo O, Victor SR, Pagnocca FC, Bueno OC, Hebling MJA (2001) Triterpene benzoates from the bark of Picramnia teapensis (Simaroubaceae). J Braz Chem Soc 12:386–390. https://doi.org/10.1590/S0103-50532001000300010
Sartor CFP, Lima MP, Silva MFGF, Fernandes JB, Forim MR, Pirani JR (2019) New limonoids from Dictyoloma vandellianum and Sohnreyia excelsa: chemosystematic considerations. J Braz Chem Soc 30:2464–2476
Scholz H (1964) Sapindales. In: Melchior H (ed) Engler's Syllabus der Pflanzenfamilien, 12th edn. Gebriider Bomtriiger, Berlin, vol 2, 267–268
Severino VGP, Braga PAC, Silva MFGF, Fernandes JB, Vieira PC, Theodoro JE, Ellena JÁ (2012) Cyclopropane- and spirolimonoids and related compounds from Hortia oreadica. Phytochemistry 76:52–59. https://doi.org/10.1016/j.phytochem.2011.12.016
Silva MFGF, Gottlieb OR (1987) Evolution of quassinoids and limonoids in the Rutales. Biochem Syst Ecol 15:85–103. https://doi.org/10.1016/0305-1978(87)90086-X
Silva MFGF, Gottlieb OR, Dreyer DL (1984) Evolution of limonoids in the Meliaceae. Biochem Syst Ecol 12:299–310. https://doi.org/10.1016/0305-1978(84)90053-X
Silva MFGF, Gottlieb OR, Ehrendorfer F (1988) Chemosystematics of the Rutaceae: suggestions for a more natural taxonomy and evolutionary interpretation of the family. Plant Syst Evol 161:97–134. https://doi.org/10.1007/BF00937293
Silva RR, Wang M, Nothias LF, Hooft JJJ, Carvalho-Rodríguez AM, Fox E, Balunas MJ, Klassen JL, Lopes NP, Dorrestein PC (2018) Propagating annotations of molecular networks using in silico fragmentation. PLoS Comput Biol. https://doi.org/10.1371/journal.pcbi.1006089
Simao SM, Barreiros EL, Silva MFGF, Gottlieb OR (1991) Chemogeographical evolution of quassinoids in Simaroubaceae. Phytochemistry 30:853–865. https://doi.org/10.1016/0031-9422(91)85267-4
Solis PN, Ravelo AG, Gonzáles AG, Gupta MP, Phillipson JD (1995) Bioactive anthraquinone glycosides from Picramnia antidesma ssp. Fessonia. Phytochemistry 38:477–480. https://doi.org/10.1016/0031-9422(94)00598-n
Suárez LEC, Casabó J, Monache FD, Molins E, Espinosa E, Miravitlles C (1998) Hortialide A, a novel limonoid from Hortia colombiana. An Quim 94:307–310 (ISSN 1130–2283, CODEN AQIEFZ)
Suárez LEC, Menichini F, Monache FD (2002) Tetranorterpenoids and dyhydrocinnamic acid from Hortia colombiana. J Braz Chem Soc 13:339–344. https://doi.org/10.1590/S0103-50532002000300008
Tan QG, Luo XD (2011) Meliaceous limonoids: Chemistry and biological activities. Chem Rev 111:7437–7522
Thomas WW (2011) Nothotalisia, a new genus of Picramniaceae from tropical America. Brittonia 63:51–61. https://doi.org/10.1007/s12228-010-9130-8
Tobe H (2011) Embryological evidence supports the transfer of Leitneria floridana to the family Simaroubaceae. Ann Mo Bot Gard 98:277–293. https://doi.org/10.3417/2009073
Vieira IJC, Braz-Filho R (2006) Quassinoids: structural diversity, biological activity and synthetic studies. Stud Nat Prod Chem 33:433–492. https://doi.org/10.1016/S1572-5995(06)80032-3
Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, Nguyen DD, Watrous J, Kapono CA, Luzzatto-Knaan T et al (2016) Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat Biotechnol 34:828–837. https://doi.org/10.1038/nbt.3597
Waterman PG (1993) Phytochemical diversity in the order Rutales. In: Downum KR, Romeo JT, Stafford HA (eds) Phytochemical potential of tropical plants. Plenum Press, New York, pp 203–233
Yan X-H, Di Y-T, Fang X, Yang S-Y, He H-P, Li S-L, Lu Y, Hao X-J (2011) Chemical constituents from fruits of Harrisonia perforate. Phytochemistry 72:508–5013. https://doi.org/10.1016/j.phytochem.2011.01.010
Yan X-H, Yi P, Cao P, Yang S-Y, Fang X, Zhang Y, Wu B, Leng Y, Di Y-T, Lv Y, Hao XJ (2016) 16-nor Limonoids from Harrisonia perforata as promising selective 11β-HSD1 inhibitors. Sci Rep 6:36927. https://doi.org/10.1038/srep36927
Yuan C-M, Zhang Y, Tang G-H, Di Y-T, Cao M-M, Wang X-Y, Zuo G-Y, Li S-L, Hua H-M, He H-P, Hao X-J (2013) Khayseneganins A-H, Limonoids from Khaya senegalensis. J Nat Prod 76:327–333. https://doi.org/10.1021/np3006919
Zhang Y, Xu H (2017) Recent progress in the chemistry and biology of limonoids. RSC Adv 7:35191–35220. https://doi.org/10.1039/c7ra04715k
Zhou Y, Lv H, Wang W, Tu P, Jiang Y (2014) Flavonoids and anthraquinones from Murraya tetramera C. C. Huang (Rutaceae). Biochem Syst Ecol 57:78–80. https://doi.org/10.1016/j.bse.2014.07.016
Acknowledgements
This work was supported by grants from FAPESP (2014/50918-7; 2012/25299-6), FAPESP-GlaxoSmithKline (2014/50249-8), CNPq (465357/2014-8), and CAPES (88887.136357/2017-00).
Author information
Authors and Affiliations
Contributions
L da SP, JCA, and DF da S reviewed the literature reports on the limonoids, quassinoids, chromones, and anthraquinones obtained up to now from species belonging to the Rutaceae, Meliaceae, Simaroubaceae, and Picramniaceae families. The experiments on UPLC-QTOF-MS/MS and GNPS were carried out by Luciano S Pinto. The data were analyzed by Maria Fátima das Graças Fernandes da Silva, Moacir Rossi Forim, and João Batista Fernandes. All authors read, edited and approved the manuscript.
Corresponding author
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
About this article
Cite this article
Fernandes da Silva, M.F.G., da Silva Pinto, L., Amaral, J.C. et al. Nortriterpenes, chromones, anthraquinones, and their chemosystematics significance in Meliaceae, Rutaceae, and Simaroubaceae (Sapindales). Braz. J. Bot 45, 15–40 (2022). https://doi.org/10.1007/s40415-021-00733-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-021-00733-9