ZYGOPHYLLALES Chalk

Takhtajan, Sist. Filog. Cvetk. Rast. [Syst. Phylog. Magnolioph.]: 264. 4 Feb 1967

Rosopsida Batsch, Tab. Regni Veg.: 1. 1802 [’Rosaceae’]; Hamamelididae Takht, Sist. Filog. Cvetk. Rast. [Syst. Phylog. Magnolioph.]: 461. 4 Feb 1967, pro parte; Rosidae Takht., Sist. Filog. Cvetk. Rast. [Syst. Phylog. Magnolioph.]: 264. 4 Feb 1967 pro parte; Dilleniidae Takht. ex Reveal et Takht. in Phytologia 74: 171. 25 Mar 1993, pro parte

FABIDAE W. S. Judd, D. E. Soltis et P. S. Soltis

ZYGOPHYLLALES Link

Habit Usually bisexual (rarely dioecious), usually evergreen shrubs, suffrutices, or perennial or annual herbs (rarely trees), sometimes with axillary, simple or branched, spines. Often xerophytes or halophytes. C₄-photosynthesis present.

Vegetative anatomy Mycorrhiza probably absent. Phellogen ab initio superficially or deeply seated (pericyclic to deep cortical). Vessel elements with simple perforation plates; lateral pits alternate, bordered pits. Imperforate tracheary elements tracheids or fibre tracheids with simple or bordered pits, non-septate (also vasicentric tracheids). Wood rays uniseriate or multiseriate, homocellular or heterocellular. Axial parenchyma usually apotracheal diffuse, diffuse-in-aggregates or banded (rarely paratracheal scanty vasicentric). Sieve tube plastids usually S type (rarely Pcs type, with two unequally sized protein crystalloids). Nodes 1:1 or 3:3, unilacunar with one leaf trace or trilacunar with three traces. Parenchyma often with sclerenchymatous idioblasts. Tanniniferous secretory cells sometimes present. Dark-brown substances present in heartwood in some species (e.g. Guaiacum officinale). Calciumoxalate present as druses or styloids, prismatic or acicular crystals, often in idioblasts.

Trichomes Hairs usually unicellular (sometimes multicellular), simple or furcate (rarely peltate or capitate); glandular hairs rarely present.

Leaves Usually alternate (spiral) or opposite, usually pinnately compound (rarely unifoliolate, bifoliolate or trifoliolate), leaflets entire, usually persistent (rarely caducous), often coriaceous, sometimes succulent or modified into spines, with ? ptyxis. Stipules cauline or interpetiolar (sometimes modified into spines) or absent; leaf sheath absent. Petiole vascular bundle transection arcuate or annular. Venation usually pinnate (rarely palmate, leaves sometimes uninerved), eucamptodromous or brochidodromous. Stomata usually anomocytic or paracytic (rarely cyclocytic or actinocytic), sometimes transversely orientated. Cuticular wax crystalloids at least sometimes as platelets. Epidermis and mesophyll sometimes with mucilaginous idioblast. Tannins and crystals often frequent. Lamina rarely gland-dotted. Leaves or leaflet margins entire.

Inflorescence Usually axillary (sometimes terminal or leaf-opposite), usually few-flowered cymose or racemose of different shape, or flowers solitary axillary. Floral prophylls (bracteoles) small or absent.

Flowers Usually actinomorphic or zygomorphic. Usually hypogyny (rarely half epigyny). Sepals (four or) five (or six), with imbricate or valvate aestivation, sometimes caducous, usually free (rarely connate at base). Petals (four or) five (or six), usually with imbricate aestivation, often clawed, usually free (sometimes partially connate). Disc annular or intrastaminal and lobate, or absent, sometimes also with extrastaminal and/or intrastaminal nectariferous glands.

Androecium Stamens usually four, eight or ten (sometimes three, five or twelve), in one or two whorls, antesepalous and/or alternisepalous (antesepalous whorl sometimes consisting of staminodia or absent). Filaments sometimes winged, sometimes with scales or other appendages at base, free or connate at base, usually free from tepals. Anthers dorsifixed or basifixed, versatile or non-versatile, tetrasporangiate, introrse to latrorse, longicidal (dehiscing by longitudinal slits) or poricidal (dehiscing by apical pores or short slits). Tapetum secretory. Staminodia usually absent (extrastaminal antesepalous staminal whorl or median abaxial stamen rarely staminodial).

Pollen grains Microsporogenesis simultaneous. Pollen grains usually tricolporate (sometimes tricolpate, tricolporoidate, tetracolporate, triporate, synorate, or polypantoporate, rarely hexarugorate), shed as monads, bicellular or tricellular at dispersal. Exine tectate or semitectate, with columellate infratectum, usually reticulate (sometimes striate, rarely rugulate, columellate or retipilate).

Gynoecium Pistil composed of two to five (or six) connate antepetalous carpels. Ovary usually superior (rarely semi-inferior), bilocular or (quadrilocular or) quinquelocular (to duodecemlocular); locules sometimes divided by secondary septa. Style single, simple (sometimes gynobasic). Stigma punctate, capitate, clavate or as commissural ridges down style, papillate, Dry or Wet type. Pistillodium absent.

Ovules Placentation axile(-marginal; sometimes apical). Ovules usually one to ten (sometimes more than ten) per carpel, usually anatropous (rarely campylotropous, hemianatropous or orthotropous), pendulous, epitropous, bitegmic, weakly crassinucellar. Micropyle bistomal or endostomal. Megagametophyte monosporous, Polygonum type. Endosperm development ab initio nuclear. Endosperm haustoria? Embryogenesis usually solanad (rarely caryophyllad).

Fruit Usually a loculicidal and/or septicidal capsule (sometimes a nutlike capsule or a schizocarp with two or five nutlike mericarps; rarely a drupe).

Seeds Aril usually absent. Seed coat usually testal or exotestal (rarely endotegmic). Exotesta often palisade, sometimes with enlarged tanniniferous cells. Endotesta with crystals, often lignified. Exotegmen? Endotegmic cells periclinally elongate, lignified. Perisperm not developed. Endosperm usually absent (sometimes oily). Embryo straight or somewhat curved, well differentiated, at least sometimes with chlorophyll. Cotyledons two. Germination phanerocotylar or cryptocotylar.

Phytochemistry Flavonols (kaempferol, quercetin), methylated flavonoids, ethereal oils (sesquiterpenes etc., in wood), oleanolic acid derivatives, tannins, phlobaphene, indole and quinazoline alkaloids (harman alkaloids, e.g. harmane, harmine, harmol), steroidal and triterpene saponins, anthraquinones, lignans, neolignans, nor-neolignans, pinitol, apiitol, and N-methyltyrosine present. Ellagic acid, tannins, proanthocyanidins, and cyanogenic compounds not found.

Systematics Zygophyllales may be sister-group to [‘Nitrogen fixing clade’+’COM clade’] (Soltis & al. 2011). Zhao & al. (2016) recovered a sister-group relationship between either Zygophyllales and Myrtales, or between Zygophyllales and [the COM clade+malvids].

Krameriales Kunth in C. F. P. von Martius, Consp. Regn. Veg.: 44. Sep-Oct 1835 [’Krameriaceae’]

Habit Bisexual, usually shrubs or suffrutices (Krameria lanceolata is a perennial herb, usually with woody rhizome). Root hemiparasites.

Vegetative anatomy Mycorrhiza absent. Phellogen ab initio deeply seated (sometimes in pericycle). Vessel elements with simple perforation plates; lateral pits alternate, bordered pits. Non-vestured pits present? Imperforate tracheary xylem elements (fibre?)tracheids with bordered pits, non-septate (also vasicentric tracheids). Wood rays usually uniseriate (rarely biseriate), homocellular. Axial parenchyma apotracheal diffuse or diffuse-in-aggregates, or paratracheal scanty, or banded. Wood elements sometimes (axial parenchyma) partially storied. Wood fluorescent? Phloem non-lignified. Sieve tube plastids S type. Nodes 1:1, unilacunar with one leaf trace. Parenchyma with tanniniferous secretory cells. Rhomboidal calciumoxalate crystals present especially in secondary phloem.

Leaves Leaves alternate (spiral), usually simple? (in reality unifoliolate?, rarely trifoliolate), entire, small, with ? ptyxis. Stipules and leaf sheath absent. Petiole vascular bundle transection arcuate (hippocrepomorphic, sometimes almost circular). Venation pinnate? Stomata usually paracytic (sometimes anomocytic). Cuticular wax crystalloids as narrow platelets. Mesophyll with sclerenchymatous idioblasts with sclereids and calciumoxalate druses. Tannins and crystals abundant. Leaf(let) margin entire.

Inflorescence Terminal or axillary, raceme-like or botryoid-paniculate, or flowers solitary axillary. Floral prophylls (bracteoles) foliaceous, small.

Flowers Zygomorphic, probably inverted. Pedicel articulated. Hypogyny. Sepals (four or) five, with imbricate aestivation, petaloid inside, free; median sepal abaxial, larger than remainder; three outer sepals larger than two inner sepals, often almost enclosing remaining parts of flower. Petals (four or) five, with imbricate aestivation; median petal adaxial; (two or) three adaxial petals long-clawed, usually connate at base into velum; two abaxial petals often modified into sessile glands, excreting bee-attracting lipids (free β-acetoxy fatty acids) from elaiophores in epidermis. Nectary absent. Disc absent.

Androecium Stamens (three or) four, adaxial, antesepalous, alternipetalous. Filaments stout, usually connate at base, usually free from petals (sometimes adnate to claws of adaxial petals). Anthers basifixed, curved, non-versatile, tetrasporangiate, introrse, poricidal (dehiscing by one or two apical pores or short slits). Tapetum? Staminodia usually absent (median abaxial stamen rarely staminodial).

Pollen grains Microsporogenesis simultaneous? Pollen grains tricolporate, tetracolporate, triporate or synorate, shed as monads, ?-cellular at dispersal. Exine tectate, with columellate infratectum, striate.

Gynoecium Pistil composed of two connate carpels; adaxial carpel early degenerating. Ovary superior, unilocular (pseudomonomerous, first bilocular). Style single, simple, stout, curved. Stigma small, punctate, sunken, type? Pistillodium absent.

Ovules Placentation apical. Ovules two per carpel, collateral, anatropous, pendulous, bitegmic, weakly crassinucellar. Micropyle endostomal. Outer integument approx. six cell layers thick. Inner integument four or five cell layers thick. Megagametophyte monosporous, Polygonum type. Endosperm development? Endosperm haustoria? Embryogenesis?

Fruit A one-seeded nutlike capsule with hairs and barbed spines; thin pericarp irregularly dehiscing.

Seeds Aril absent. Seed coat exotestal. Exotestal cells enlarged, tanniniferous. Endotesta? Tegmen up to seven cell layers thick above, mostly degenerating. Perisperm not developed. Endosperm absent. Embryo straight, well differentiated, chlorophyll? Haustoria formed from young adventitious roots. Cotyledons two, large, ventrally flattened, cordate. Germination? Seedling without root hairs.

Phytochemistry Tannins of catechin type, phlobaphene (red root pigment), neolignans, nor-neolignans, apiitol, and N-methyltyrosine present. Saponins not found. Harman-alkaloids?

Brown in Flinders, Voy. Terra Austral. 2: 545. 19 Jul 1814 [’Zygophylleae’], nom. cons.

Balanitaceae M. Roem., Fam. Nat. Syn. Monogr. 1:26. 14 Sept-15 Oct 1846 [‘Balaniteae’], nom. cons.; Zygophyllineae J. Presl in Nowočeská Bibl. [Wšobecný Rostl.] 7: 265, 266. 1846 [‘Zygophylleae’]; Tribulaceae Trautv., Estestv. Istorija Gub. Kievsk. Uchebn. Okr. Bot. Sist.: 28. 1853; Balanitales C. Y. Wu in Acta Phytotaxon. Sin. 40: 314. 2002

Distribution Mainly tropical and subtropical regions on both hemispheres, with their largest diversity in arid and subarid areas; some species in warm-temperate regions.

Habit Usually bisexual (rarely dioecious), evergreen shrubs, suffrutices, or perennial or annual herbs (rarely trees), sometimes with axillary, simple or branched, spines. Nodes often swollen and/or articulated. Bark often bitter. Some species are succulent. Many species are xerophytes or halophytes. C₄ photosynthesis present (almost all species in Kallstroemia have C₄ photosynthesis; nearly all in Zygophyllum are C₃ photosynthetic).

Vegetative anatomy Mycorrhiza usually absent (arbuscular mycorrhiza sometimes present in Larrea). Phellogen ab initio usually superficially (sometimes deeply) seated. Primary vascular tissue cylinder without separate vascular bundles. Primary medullary rays usually narrow (in Balanites wide). Secondary lateral growth normal or anomalous. Vessel elements with simple perforation plates; lateral pits alternate, bordered pits. Vestured pits present. Imperforate tracheary elements tracheids or fibre tracheids (or libriform fibres?) with simple and/or bordered pits, non-septate (also vasicentric tracheids). Wood rays uniseriate or multiseriate, one or two (to four) cells wide (in Balanites up to c. 35 cells wide), homocellular or heterocellular. Axial parenchyma usually apotracheal diffuse, diffuse-in-aggregates or in uniseriate bands (rarely paratracheal scanty vasicentric). Wood elements usually storied. Wood often fluorescent. Sieve tube plastids usually S type (rarely Pcs type, with two unequally sized protein crystalloids). Nodes usually 1:1, unilacunar with one leaf trace, often also with split laterals (trilacunar nodes present in Viscainoa). Cortex and parenchyma often with fibres and sclerenchymatous idioblasts. Secretory cavities absent. Dark-brown substances present in heartwood in some species (e.g. Guaiacum officinale). Calciumoxalate present as druses and styloid, prismatic and acicular crystals, often in idioblasts.

Trichomes Hairs usually unicellular (sometimes multicellular), simple or furcate (rarely peltate or capitate); glandular hairs present in Fagonia.

Leaves Usually opposite (in Morkillia and Viscainoa alternate, spiral), usually pinnately compound (rarely bifoliolate or trifoliolate or probably seemingly simple: unifoliolate?), leaflets entire, usually persistent (rarely caducous), often coriaceous, sometimes succulent or modified into spines, with usually flat ptyxis. Stipules cauline or one interpetiolar (sometimes modified into spines; rarely absent); leaf sheath absent. Petiole vascular bundle transection annular; petiole with wing bundles. Venation usually pinnate (rarely palmate, leaves sometimes one-veined), eucamptodromous or brochidodromous. Stomata usually anomocytic (rarely paracytic, cyclocytic or actinocytic). Cuticular wax crystalloids? Epidermis sometimes with mucilaginous idioblasts. Mesophyll with or without sclerenchymatous idioblasts. Lamina rarely gland-dotted. Leaflet margins usually entire (sometimes serrate).

Inflorescence Usually axillary (sometimes terminal or leaf-opposite), few-flowered cymose or racemose of different appearance, or flowers solitary. Floral prophylls (bracteoles) absent.

Flowers Usually actinomorphic (rarely zygomorphic). Usually hypogyny (rarely partially perigynous). Sepals (four or) five (or six), with imbricate or valvate aestivation, sometimes caducous, usually free (rarely connate at base). Petals (four or) five (or six), usually with imbricate (or contorted?) aestivation, often clawed, free (absent in Seetzenia and one species of Zygophyllum). Disc annular or as intrastaminal lobes or absent, sometimes also with extrastaminal and/or intrastaminal nectariferous glands.

Androecium Stamens usually eight or ten (sometimes five or twelve), in one or two whorls, antesepalous and/or alternisepalous (antesepalous whorl staminodial or absent), often obdiplostemonous. Filaments sometimes winged, sometimes with scales or other appendages at base, free from each other and from tepals. Anthers dorsifixed, versatile, tetrasporangiate, introrse or latrorse, longicidal (dehiscing by longitudinal slits). Tapetum secretory. Staminodia usually absent (extrastaminal antesepalous staminal whorl rarely staminodial).

Pollen grains Microsporogenesis simultaneous. Pollen grains usually tricolporate (sometimes tricolpate, tricolporoidate or polypantoporate, rarely hexarugorate), shed as monads, bicellular or tricellular at dispersal. Exine semitectate, with columellate infratectum, usually reticulate (rarely rugulate, columellate or retipilate).

Gynoecium Pistil composed of (two to) five (or six) connate antepetalous carpels. Ovary usually superior (rarely semi-inferior), (quadrilocular or) quinquelocular (to duodecemlocular), often angular or winged (sometimes stipitate, with gynophore); locules sometimes divided by secondary septa. Style single, simple, short to long, narrow (in Zygophyllum gynobasic). Stigma capitate, punctate, clavate or as commissural ridges down style, papillate, Dry or Wet type. Pistillodium absent?

Ovules Placentation axile(-marginal; rarely apical). Ovules usually one to ten (sometimes more than ten) per carpel, usually anatropous (rarely campylotropous, hemianatropous or orthotropous), pendulous, epitropous (sometimes apotropous?), bitegmic, weakly crassinucellar. Micropyle endostomal or bistomal, usually not Z-shaped (in Balanites zig-zag). Outer integument two to six (to eight) cell layers thick. Inner integument two to four (to six) cell layers thick. Obturator present. Hypostase present. Endothelium usually present (absent in Seetzenia). Parietal tissue one or two (to four) cell layers thick. Nucellar cap sometimes present. Archespore sometimes multicellular. Megagametophyte monosporous, Polygonum type, elongated. Endosperm development ab initio nuclear. Endosperm haustoria? Embryogenesis usually solanad (rarely caryophyllad).

Fruit Usually a loculicidal and/or septicidal capsule (sometimes a schizocarp with two or five nutlike mericarps; in Balanites a one-seeded drupe with oily mesocarp).

Seeds Aril usually absent. Seed coat usually testal (rarely endotegmic). Exotesta often palisade. Endotesta usually crystalliferous, often lignified. Exotegmen? Endotegmic cells periclinally elongate, lignified. Perisperm not developed. Endosperm usually absent (sometimes present, oily). Embryo straight or somewhat curved, at least sometimes with chlorophyll. Cotyledons two. Germination phanerocotylar or cryptocotylar.

Phytochemistry Flavonoids (kaempferol, quercetin, isorhamnetin-3-rutinoside in Zygophyllum), methylated flavonoids, ethereal oils (sesquiterpenes etc., in wood), oleanolic acid derivatives, quinazoline alkaloids (harmane, harmin, harmol and other harmala alkaloids), indole alkaloids, steroidal and triterpene saponins, anthraquinones, lignans, neolignans, and pinitol present. Ellagic acid, tannins, proanthocyanidins, and cyanogenic compounds not found. Mustard oils?

Use Ornamental plants, timber and carpentries (extremely hard wood, Lignum vitae, from Guaiacum), fruits (Balanites aegyptiaca), medicinal plants, edible flower buds.

Systematics Zygophyllaceae are sister-group to Krameria (Krameriaceae).

[[Morkillioideae+Balanitoideae]+[Seetzenioideae+[Larreoideae+Zygophylloideae]]] is a plausible topology (Sheahan & Case 2000).

[Morkillioideae+Balanitoideae]

Morkillioideae Thorne et Reveal in Bot. Rev. (Lancaster) 73: 106. 29 Jun 2007

3/4. Morkillia (2; M. acuminata, M. mexicana; Mexico), Viscainoa (1; V. geniculata; Baja California in northwestern Mexico), Sericodes (1; S. greggii; northern Mexico). – Mexico. Leaves usually alternate (spiral).

Balanitoideae Engl. in Engler et Prantl, Nat. Pflanzenfam. III, 4: 354, 355. Jul 1896

6/80–90. Tribulus (40–45; tropical and subtropical regions on both hemispheres), Kallstroemia (30–35; tropical and subtropical America), Kelleronia (3; K. gillettiae, K. revoilii, K. splendens; northeastern Africa, southern Arabian Peninsula), Sisyndite (1; S. spartea; southern Namibia, Northern and northwestern Western Cape), Neoluederitzia (1; N. sericeocarpa; southern Namibia), Balanites (9; tropical Africa, the Arabian Peninsula to India and Burma). – Tropical to warm-temperate regions on both hemispheres. C₄ photosynthesis frequent in Kallstroemia. Fruit usually a schizocarp with four or five or up to ten single-seeded nutlike mericarps. – Balanites are spiny shrubs or trees with bitter bark. Medullary and wood rays very wide. Stipules tiny (absent?). Petiole anatomy complicated. Stem stomata transversely orientated relative to longitudinal axis. Leaves alternate (spiral) and pinnately compound with one pair of leaflets. Corolla enclosing floral bud. Ovule one per carpel, pendulous. Micropyle bistomal, Z-shaped (zig-zag). Outer integument four to eight cell layers thick. Inner integument three to six cell layers thick. Fruit a single-seeded drupe. Endosperm absent. Testa multiplicative, vascularized.

[Seetzenioideae+[Larreoideae+Zygophylloideae]]

Seetzenioideae M. C. Sheahan et M. W. Chase in Bot. J. Linn. Soc. 122: 299. 18 Dec 1996

1/1. Seetzenia (1; S. lanata; North Africa to Afghanistan and India, Northern and Eastern Cape). – Prostrate perennial herb. Leaves opposite, trifoliolate. Petals absent. Stamens five. Filaments without scale-like processes. Carpels five. Stylidia five. Ovule one per carpel, epitropous. Micropyle bistomal. Outer integument six or seven cell layers thick. Endothelium absent. Fruit a septicidal capsule, dehiscing into five single-seeded cocci with fleshy exocarp and bony endocarp. Endosperm present.

[Larreoideae+Zygophylloideae]

Larreoideae M. C. Sheahan et M. W. Chase in Bot. J. Linn. Soc. 122: 299. 18 Dec 1996

8/32–36. Bulnesia (8–10; South America), Guaiacum (8–10; tropical and subtropical America), Porlieria (5; P. angustifolia, P. arida, P. chilensis, P. hygrometra, P. microphylla; Mexico, the Andes), Larrea (6; L. ameghinoi, L. cuneifolia, L. divaricata, L. nitida, L. simulans, L. tridentata; southwestern United States, Mexico, South America), Pintoa (1; P. chilensis; Chile), Plectrocarpa (2; P. rougesii, P. tetracantha; temperate South America), Metharme (1; M. lanata; northern Chile); unplaced: Izozogia (1; I. nellii; Bolivia). – Southwestern United States, Mexico, Central and South America to Chile and Argentina. Sieve tube plastids in Larrea with protein and starch. Filaments often with scale-like processes. Ovary stipitate or sessile. Capsule often winged. Seed one per locule. Endosperm present.

Zygophylloideae Arn., Botany: 104. 9 Mar 1832 [‘Zygophylleae’]

1/80–85. Zygophyllum (80–85; Macaronesia, the Mediterranean, southeastern Europe, northern and northeastern Africa to Iran, Central Asia and northwestern India, China, tropical and subtropical to southern Africa, Australia, southwestern United States, Mexico). – Mainly drier regions of the Old World, southwestern United States, Chile. Nectariferous disc octa- or decemangulate. Stamens eight or ten. Filaments with basal scale-like processes. Style in Zygophyllum simple, gynobasic. Stigma punctate. Outer and inner integuments in Zygophyllum approx. two cell layers thick. Fruit an angular to winged capsule or schizocarp.

Cladogram (simplified) of Zygophyllaceae based on DNA sequence data (Sheahan & Chase 2000).

Achenbach H, Gross J, Dominguez XA, Cano G, Star JV, Brussolo L d C, Muñoz FSG, López L. 1987. Lignans, neolignans, and nor-neolignans from Krameria cytisoides. – Phytochemistry 26: 1159-1166.

Achenbach H, Gross J, Dominguez XA, Star JV, Salgado F. 1987. Ramosissin and other methoxylated nor-neolignans from Krameria ramosissima. – Phytochemistry 26: 2041-2043.

Achenbach H, Gross J, Bauereiss P, Dominguez XA, Vega HS, Star JV, Rombold C. 1989. Nor-lignans and nor-neolignans from Krameria lanceolata. – Phytochemistry 28: 1959-1962.

Agababyan VS. 1964. Morphological types of pollen and systematic classification of the Zygophyllaceae. – Izv. Akad. Nauk Armyanskoi, SSR, Biol. Nauk 17: 39-45. [In Russian]

Axelrod FS. 2002. Proposal to conserve the name Guaiacum (Zygophyllaceae) with that spelling. – Taxon 51: 203-204.

Barker RJ. 1996. New taxa, new combinations, keys and comments on generic concepts of Zygophyllum and a new species of Tribulus (Zygophyllaceae) in the manuscripts of the late H. J. Eichler. – J. Adelaide Bot. Gard. 17: 161-172.

Barker RJ. 1998a. Notes on the genus Tribulopsis (Zygophyllaceae) in Australia. – J. Adelaide Bot. Gard. 18: 77-93.

Barker RJ. 1998b. A trial key and notes on Tribulus (Zygophyllaceae) in Australia, including one new species and validation of Tribulus suberosus. – Nuytsia 12: 9-35.

Behnke H-D. 1988. Sieve-element plastids and systematic relationships of Rhizophoraceae, Anisophylleaceae and allied groups. – Ann. Missouri Bot. Gard. 75: 1387-1409.

Beier B-A. 2005. A revision of the desert shrub Fagonia (Zygophyllaceae). – Syst. Biodivers. 3: 221-263.

Beier B-A, Thulin M. 2004. Proposal to conserve the name Tetraena against Petrusia (Zygophyllaceae). – Taxon 53: 1078-1079.

Beier B-A, Chase MA, Thulin M. 2003. Phylogenetic relationships and taxonomy of subfamily Zygophylloideae (Zygophyllaceae) based on molecular and morphological data. – Plant Syst. Evol. 240: 11-39.

Beier B-A, Nylander JAA, Chase MA, Thulin M. 2004. Phylogenetic relationships and biogeography of the desert plant genus Fagonia (Zygophyllaceae), inferred by parsimony and Bayesian model averaging. – Mol. Phylogen. Evol. 33: 91-108.

Bellstedt DU, Zyl L van, Marais EM, Bytebier B, Villiers CA de, Makwarela AM, Dreyer LL. 2008. Phylogenetic relationships, character evolution and biogeography of southern African members of Zygophyllum (Zygophyllaceae) based on three plastid regions. – Mol. Phylogen. Evol. 47: 932-949.

Bellstedt DU, Zyl L van, Marais EM, Bytebier B, Villiers CA de, Dreyer LL, Galley C, Pirie M, Linder HP. 2008. A molecular phylogeny reveals evidence of rapid and recent radiation in Cape and Australian members of the genus Zygophyllum. – South Afr. J. Bot. 74: 361.

Bellstedt DU, Galley C, Pirie MD, Linder HP. 2012. The migration of the Palaeotropical arid flora: Zygophylloideae as an example. – Syst. Bot. 37: 951-959.

Boesewinkel FD. 1994. Ovules and seed characters of Balanites aegyptiaca and the classification of the Linales-Geraniales-Polygalales assembly. – Acta Bot. Neerl. 43: 15-25.

Busse-Jung F. 1979. Phytoserologische Untersuchungen zur Frage der systematischen Stellung von Krameria triandra Ruiz et Pav. – Ph.D. diss., Christian-Albrechts-Universität, Kiel, Germany.

Cannon WA. 1910. The root habits and parasitism of Krameria canescens Gray. – In: MacDougall DT, Cannon WA (eds), The conditions of parasitism in plants, Publ. Carnegie Inst. Washington 129: 5-24.

Carlquist SJ. 2005. Wood anatomy of Krameriaceae with comparisons with Zygophyllaceae: phylesis, ecology and systematics. – Bot. J. Linn. Soc. 149: 257-270.

Carranco ME, Perez GF. 1989. A study on the chemical composition and toxicological factors of Guayacan Viscainoa geniculata. – Cuban J. Agricult. Sci. 23: 333-336.

Chodat M. 1890. Un travail monographique sur la famille des Kramériacées. – Arch. Sci. Phys. Nat. 24: 495-499.

Crisci JV, Hunziker JH, Palacios RA, Naranjo CA. 1979. A numerical-taxonomic study of the genus Bulnesia (Zygophyllaceae): cluster analysis, ordination and simulation of evolutionary trees. – Amer. J. Bot. 66: 133-140.

Crookston RK, Moss DN. 1972. C₄ and C₃ carboxylation characteristics in the genus Zygophyllum. – Ann. Missouri Bot. Gard. 59: 465-470.

Descole HR, O’Donnell CA, Lourteig A. 1940. Revisión de las Zygofiláceas Argentinas. – Lilloa 5: 257-343.

Dhillon M. 1976. Vascular anatomy of the flower of Krameria Parvifolia var. glandulosa Macbr. and its bearing on its taxonomic status. – J. Res. Punjab Agric. Univ. 13: 197-201.

Domínguez XA, Espinoza BG, Rombold C, Utz W, Achenbach H. 1992. Neolignans, norneolignans, and other compounds from Krameria sonorae. – J. Med. Plant Res. 58: 382-383.

Eichler H. 1990. Four new species of Zygophyllum (Zygophyllaceae) and one lectotypification. – Telopea 4: 13-17.

El Hadidi MN. 1972a. Neue Beobachtungen an der Gattung Fagonia L. – Candollea 27: 85-96.

El Hadidi MN. 1972b. The family Zygophyllaceae in Egypt I. Fagonia L. and Seetzenia R. Br. – Bot. Not. 125: 523-535.

El Hadidi MN. 1973. Revision of Fagonia species (Zygophyllaceae) with tri- to unifoliolate and simple leaves. – Österr. Bot. Zeitschr. 121: 269-278.

El Hadidi MN. 1977a. Tribulaceae as a distinct family. – Publ. Cairo Univ. Herb. 7-8: 103-108.

El Hadidi MN. 1977b. Two new Zygophyllum species from Arabia. – Publ. Cairo Univ. Herb. 7-8: 327-331.

El Hadidi MN. 1978a. The genus Zygophyllum in Egypt. – Bot. Not. 131: 439-443.

El Hadidi MN. 1978b. Adumbratio florae aethiopicae: Zygophyllaceae. – Webbia 33: 45-101.

El Hadidi MN. 1985. Zygophyllaceae. – In: Polhill RM (ed), Flora of tropical East Africa, A. A. Balkema, Rotterdam, pp. 1-15.

El Naggar SM, Abdel-Hafez SII. 2007. Pollen morphology, leaf surfaces, mycobiota diversity and leaf spots of three species of Zygophyllum growing along Cairo-Suez desert road, Eastern (Arabian) desert in Egypt. – Feddes Repert. 118: 38-45.

Engler A. 1896a. Zygophyllaceae. – In: Engler A, Prantl K (eds), Die natürlichen Pflanzenfamilien III(4), W. Engelmann, Leipzig, pp. 74-93.

Engler A. 1896b. Über die geographische Verbreitung der Zygophyllaceen. – Königliche Akademie der Wissenschaften, Berlin.

Engler A (†). 1931. Zygophyllaceae. – In: Engler A (†), Harms H, Pax F (eds), Die natürlichen Pflanzenfamilien, 2. Aufl., Bd. 19a, W. Engelmann, Leipzig, pp. 144-184.

Fahn A, Shimony C. 1996. Glandular trichomes of Fagonia L. (Zygophyllaceae) species: structure, development and secreted materials. – Ann. Bot. 77: 25-34.

Gadek PA, Fernando ES, Quinn CJ, Hoot SB, Terrazas T, Sheahan MC, Chase MW. 1996. Sapindales: molecular delimitation and infraordinal groups. – Amer. J. Bot. 83: 802-811.

Hilu KW. 1970. Cytotaxonomy of some taxa of Zygophyllaceae in Iraq. – M.Sc. thesis, University of Baghdad, Iraq.

Hilu KW. 1981. Cytotaxonomical studies in Tribulus terrestris and T. alatus (Zygophyllaceae). – Nord. J. Bot. 1: 531-534.

Hosni HA. 1977. A new Tribulus species with winged carpels. – Bot. Not. 130: 261-262.

Hunziker JH. 1975. On the geographical origin of Larrea divaricata (Zygophyllaceae). – Ann. Missouri Bot. Gard. 62: 497-500.

Hunziker JH, Palacios RA, Poggio L, Naranjo CA, Yang T-W. 1977. Geographic distribution, morphology, hybridization, cytogenetics, and evolution. – In: Mabry TJ, Hunziker JH, DiFeo DR Jr (eds), Creosote bush: biology and chemistry of Larrea in New World deserts, Dowden, Hutchinson & Ross, Stroudsburg, Pennsylvania, pp. 10-47.

Hussein SR, Kawashty SA, Tantawy ME, Saleh NAM. 2009. Chemosystematic studies of Nitraria retusa and selected taxa of Zygophyllaceae in Egypt. – Plant Syst. Evol. 277: 251-264.

Huyssteen DC van. 1937. Morphologisch-systematische Studien über die Gattung Zygophyllum. – Ph.D. diss., Math.-Naturwiss. Fakultät, Friedrich-Wilhelms-Universität, Berlin, Germany.

Inamdar JA. 1969. Epidermal structure, stomatal ontogeny, and relationship of some Zygophyllaceae and Simaroubaceae. – Flora 158B: 360-368.

Inamdar JA, Patel RC. 1970. Epidermal structure and development of stomata in vegetative and floral organs of Fagonia cretica Linn. – Flora 159B: 63-70.

Keighery GJ. 1982. Geocarpy in Tribulopsis R. Br. (Zygophyllaceae). – Flora 172: 329-333.

Kunz M. 1913. Die systematische Stellung der Gattung Krameria unter besonderer Berücksichtigung der Anatomie. – Beih. Bot. Centralbl. 30: 412-427.

Lahham JN, Al-Eisawi D. 1986. Pollen morphology of Jordanian Zygophyllaceae. – Candollea 41: 325-328.

Launert E. 1963a. 36. Zygophyllaceae. – In: Exell AW, Fernandes A, Wild H (eds), Flora Zambesiaca 2 (Part 1), Crown Agents for Oversea Governments and Administrations, London, pp. 125-130.

Launert E. 1963b. 43. Balanitaceae. – In: Exell AW, Fernandes A, Wild H (eds), Flora Zambesiaca 2 (Part 1), Crown Agents for Oversea Governments and Administrations, London, pp. 221-224.

Lauterbach M, Wet van der Merwe P de, Keßler L, Pirie MD, Bellstedt DU, Kadereit G. 2016. Evolution of leaf anatomy in arid environments – a case study in southern African Tetraena and Roepera (Zygophyllaceae). – Mol. Phylogen. Evol. 97: 129-144.

Leinfellner W. 1971. Das Gynözeum von Krameria und sie Vergleich mit jenem der Leguminosae und der Polygalaceae. – Österr. Bot. Zeitschr. 119: 102-117.

Lia VV, Confalonieri VA, Comas CI, Hunziker JH. 2001. Molecular phylogeny of Larrea and its allies (Zygophyllaceae): reticulate evolution and the probable time of the creosote bush arrival to North America. – Mol. Phylogen. Evol. 21: 309-320.

Ma Y-C, Zhang S. 1990. Study on the systematic position of Tetraena Maxim. – Acta Phytotaxon. Sin. 28: 89-95.

Mabry TJ, Hunziker JH, DiFeo DR Jr (eds), 1977a. Creosote bush: biology and chemistry of Larrea in New World deserts, Dowden, Hutchinson & Ross, Stroudsburg, Pennsylvania.

Mabry TJ, DiFeo DR Jr, Sakakibara M, Bohnstedt CF Jr, Seigler D. 1977b. The natural products of Larrea. – In: Mabry TJ, Hunziker JH, DiFeo DR Jr (eds), Creosote bush: biology and chemistry of Larrea in New World deserts, Dowden, Hutchinson & Ross, Stroudsburg, Pennsylvania, pp. 115-134.

Maksoud SA, El-Hadidi MN. 1988. The flavonoids of Balanites aegyptiaca from Egypt. – Plant Syst. Evol. 160: 153-158.

Mathur A, Bhandari MM. 1983. Studies on pollen grains of Fagonia and Seetzenia species. – J. Econ. Taxon. Bot. 4: 331-334.

Mauritzon J. 1934. Etwas über die Embryologie der Zygophyllaceen sowie einige Fragmente über die der Humiriaceen. – Bot. Not. 87: 407-422.

Milby TH. 1971. Floral anatomy of Krameria lanceolata. – Amer. J. Bot. 58: 569-576.

Mohamed AH. 2006. Taxonomic significance of seed proteins and iso-enzymes in Tribulus (Zygophyllaceae). –Intern. J. Agricult. Biol. 8: 573-575.

Musselman LJ. 1975. Parasitism and haustorial structure in Krameria lanceolata (Krameriaceae). A preliminary study. – Phytomorphology 25: 416-422.

Nag TN et al. 1986. Free endogenous ascorbic acid from Zygophyllaceous plants growing in the arid zone of Rajasthan. – J. Indian Bot. Soc. 9: 112-113.

Nair NC, Jain RK. 1956. Floral morphology and embryology of Balanites roxburghii Planch. – Lloydia 19: 269-279.

Nair NC, Nathawat KS. 1958. Vascular anatomy of the flower of some species of Zygophyllaceae 1. – J. Indian Bot. Soc. 37: 172-180.

Narayana HS, Prakasa Rao CG. 1963. Floral morphology and embryology of Seetzenia orientalis Decne. – Phytomorphology 13: 197-205.

Narayana L, Satyauarayana P, Radhakrishnaiah H. 1990. Systematic position of Balanitaceae. – In: Bilgrami K, Dogra J (eds), Phytochemistry and plant taxonomy, CBS Publ., Delhi, pp. 157-164.

Navarro G. 1997. Izozogia nellii (Zygophyllaceae), Nuevo Género y Especie del Gran Chaco de Santa Cruz (Bolivia). – Novon 7: 1-5.

O’Gara RW, Lee CW, Morton JF, Kapadia GJ, Dunham LJ. 1974. Sarcoma induced in rats by extracts of plants and by fractionated extracts of Krameria ixina. – J. Natl. Cancer Inst. 52: 445-448.

Ozenda P, Quézel P. 1956. Les Zygophyllacées de l’Afrique du Nord et du Sahara. – Trav. Inst. Rech. Sahariennes 14: 23-83.

Palacios RA, Hunziker JH. 1984. Revisión taxonómica del género Bulnesia (Zygophyllaceae). – Darwiniana 25: 299-320.

Parameswaran N, Conrad H. 1982. Wood and bark anatomy of Balanites aegyptiaca in relation to ecology and taxonomy. – IAWA Bull., N. S., 3: 75-88.

Pederiva R, Kavka J, D’Archangelo A. 1975. Chalcones and flavanones isolated from Larrea nitida. – Ann. Asoc. Quim. Argent. 63: 85-90.

Perveen A, Qaiser M. 2006. Pollen flora of Pakistan XLIX. Zygophyllaceae. – Pak. J. Bot. 38: 252-232.

Phatak VG. 1971. Embryology of Zygophyllum coccineum L. and Z. fabago L. – Proc. Kon. Nederl. Akad. Wetensch. 74C: 379-397.

Poggio L. 1978. Éstudios cromosómicos en Bulnesia, Pintoa, Porlieria, Plectrocarpa y Sericodes (Zygophyllaceae). – Darwiniana 21: 139-151.

Poggio L, Burghardt AD, Hunziker JH. 1989. Nuclear DNA variation in diploid and polyploid taxa of Larrea (Zygophyllaceae). – Heredity 63: 321-328.

Poggio L, Hunziker JH, Wulff AF. 1992. Cariotipo y contenido de ADN nuclear de Pintoa chilensis y Sisyndite spartea (Zygophyllaceae). – Darwiniana 31: 11-15.

Popov G. 1925. Generis Zygophylli species asiaticae. – Bull. Univ. l’Asie Centr. (Taschkent) 11: 105-122.

Popov G. 1926. Generis Zygophylli species asiaticae. – Bull. Univ. l’Asie Centr. (Taschkent) 12: 109-125.

Porter DM. 1963. Taxonomy and distribution of the Zygophyllaceae of Baja California, Mexico. – Contr. Gray Herb. 192: 99-135.

Porter DM. 1969. The genus Kallstroemia (Zygophyllaceae). – Contr. Gray Herb. 198: 41-153.

Porter DM. 1971. Notes on the floral glands in Tribulus (Zygophyllaceae). – Ann. Missouri Bot. Gard. 58: 1-5.

Porter DM. 1974. Disjunct distributions in the New World Zygophyllaceae. – Taxon 23: 339-346.

Porter DM. 2005. 90. Zygophyllaceae. – In: Harling G, Andersson L (eds), Flora of Ecuador 75, Botanical Institute, Göteborg University, pp.17-29.

Rose JN. 1909. Studies of Mexican and Central American plants VI. – Contr. U.S. Natl. Herb. 12: 275.

Saleh NAM, El Hadidi MN. 1977. An approach to the chemosystematics of the Zygophyllaceae. – Biochem. Syst. Ecol. 5: 121-128.

Saleh N, El Hadidi MN, Ahmed A. 1982. The chemosystematics of Tribulaceae. – Biochem. Syst. Ecol. 10: 313-317.

Sands MJS. 1983. Notes on Balanites from the Somali Republic and Ethiopia. – Kew Bull. 38: 40.

Sands MJS. 1989. Balanitaceae. – In: Hedberg I, Edwards S (eds), Flora of Ethiopia III, Addis Ababa University, Ethiopia, and Uppsala University, Sweden, pp. 433-436.

Sands MJS. 2001. The desert date and its relatives: a revision of the genus Balanites. – Kew Bull. 56: 1-128.

Sands MJS. 2003. Balanitaceae. – In: Beentje HJ, Ghazanfar SA (eds), Flora of tropical East Africa, A. A. Balkema Publ., Lisse, The Netherlands, pp. 1-14.

Sarma V, Rao SRS. 1991. Taxonomic importance of epidermis in Simaroubaceae-Zygophyllaceae with special reference to position of Balanites. – Feddes Repert. 102: 579-585.

Schweickerdt HG. 1937. An account of the South African species of Tribulus Tour. ex Linn. – Bothalia 3: 159-178.

Seigler D, Simpson BB, Martin C, Neff JL. 1978. Free 3-acetoxy fatty acids in floral glands of Krameria species. – Phytochemistry 17: 995-996.

Sheahan MC, Chase MW. 1996. A phylogenetic analysis of Zygophyllaceae R. Br. based on morphological, anatomical and rbcL DNA sequence data. – Bot. J. Linn. Soc. 122: 279-300.

Sheahan MC, Chase MW. 2000. Phylogenetic relationships within Zygophyllaceae based on DNA sequences of three plastid regions, with special emphasis on Zygophylloideae. – Syst. Bot. 25: 371-384.

Sheahan MC, Cutler DF. 1993. Contribution of vegetative anatomy to the systematics of the Zygophyllaceae R. Br. – Bot. J. Linn. Soc. 113: 227-262.

Simpson BB. 1982. Krameria (Krameriaceae) flowers: orientation and elaiophore morphology. – Taxon 31: 517-528.

Simpson BB. 1989. Flora Neotropica. Monograph 49. Krameriaceae. – New York Botanical Garden, Bronx, New York.

Simpson BB. 1991. The past and present uses of rhatany (Krameria, Krameriaceae). – Econ. Bot. 45: 397-409.

Simpson BB, Neff JL. 1978. Dynamics and derivation of the pollination syndrome of Krameria (Krameriaceae). – Bot. Soc. Amer. Misc. Publ. 156: 14.

Simpson BB, Skvarla JJ. 1981. Pollen morphology and ultrastructure of Krameria (Krameriaceae): utility in questions of intrafamilial and interfamilial classification. – Amer. J. Bot. 68: 277-294.

Simpson BB, Neff JL, Seigler DL. 1977. Krameria, free fatty acids and oil-collecting bees. – Nature 267: 150-151.

Simpson BB, Neff JL, Moldenke AR. 1977. Reproductive systems of Larrea. – In: Mabry TJ, Hunziker JH, DiFeo Dr Jr (eds), Creosote bush: biology and chemistry of Larrea in New World deserts, Dowden, Hutchinson & Ross, Stroudsberg, Pennsylvania, pp. 92-114.

Simpson BB, Seigler DS, Neff JL. 1978. Lipids from the floral glands of Krameria. – Biochem. Syst. Ecol. 7: 193-194.

Simpson BB, Weeks A, Helfgott DM, Larkin LL. 2004. Species relationships in Krameria (Krameriaceae) based on ITS sequences and morphology: implications for character utility and biogeography. – Syst. Bot. 29: 97-108.

Stahl E, Ittel I. 1981. Neue lipophile Benzofuranderivate aus Ratanhiawurzeln. – Planta Medica 42: 144-154.

Sterling CM. 1912. Krameria canescens Gray. – Kansas Univ. Sci. Bull. 6: 363-372.

Taubert P. 1892. Leguminosae II. 6. Caesalpinioideae-Kramerieae. – In: Engler A, Prantl K (eds), Die natürlichen Pflanzenfamilien, III, 3, W. Engelmann, Leipzig, pp. 166-168.

Teppner H. 1984. Karyologie von Krameria triandra (Krameriaceae). – Mitteilungsbl. Kurzfass. Beiträge, Botaniker-Tagung, 1-14 September, Wien.

Thulin M. 1993. Flora of Somalia 1. Zygophyllaceae (including Tribulaceae). – Royal Botanic Gardens, Kew.

Turner BL. 1958. Chromosome numbers in the genus Krameria: evidence for familial status. – Rhodora 60: 101-106.

Turner BL. 2016. Overview of Kallstroemia (Zygophyllaceae) in the USA and Mexico, and description of a new species: Kallstroemia porteri. – Phytologia 98: 89-99.

Verkerke W. 1985. Ovule ontogeny and seed coat development in Krameria Loefling (Krameriaceae). – Beitr. Biol. Pflanzen 60: 341-351.

Weberling F. 1956. Weitere Untersuchungen zur Morphologie des Unterblattes bei den Dikotylen III. Convolvulaceae; IV. Zygophyllaceae. – Beitr. Biol. Pflanzen 33: 149-161.

Wei N. 1991. A comparative anatomy on the vegetative organs of Tetraena mongolica Maxim. and Zygophyllum xanthoxylum (Bunge) Maxim. – Acta Scient. Natur. Univ. Intramongolicae 22: 528-533.

Wu S, Tu L. 1990. The embryology of Tetraena mongolica Maxim. – Acta Scient. Natur. Univ. Intramongolicae 21: 177-183.

Xi Y, Zhou S. 1989. Pollen morphology and its exine ultrastructure of the Zygophyllaceae in China. – Bot. Research (China) 4: 75-86.

Xi Y, Zhou S. 1992. A contribution to the pollen morphology of Tetraena and Malpighiaceae, with discussion of the affinity and taxonomic position of Tetraena. – Chinese J. Bot. 4: 6-12.

Zohary M, Orshan G. 1954. Ecological studies in the vegetation of the near eastern deserts V. The Zygophylletum dumosi and its hydroecology in the Negev of Israel. – Vegetatio 5-6: 340-350.

Zyl L van. 2000. A systematic revision of Zygophyllum (Zygophyllaceae) in the southern African region. – Ph.D. diss., University of Stellenbosch, Republic of South Africa.

Zyl L van, Marais EM. 1999. Three new species of Zygophyllum (Zygophyllaceae) from Namibia and the Northern Cape, South Africa. – Bothalia 29: 231-237.

ROSANAE Takht.

FABIDAE W. S. Judd, D. E. Soltis et P. S. Soltis

ZYGOPHYLLALES Link

KRAMERIACEAE Dumort.

ZYGOPHYLLACEAE R. Br.