Brassicaceae

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Brassicaceae
Barbarea vulgaris 002.JPG
Winter cress, Barbarea vulgaris
Scientific classification e
Kingdom: Plantae
Clade: Angiosperms
Clade: Eudicots
Clade: Rosids
Order: Brassicales
Family: Brassicaceae
Burnett[1]
Genera

See List of Brassicaceae genera

Brassicaceae (/ˌbræsɪˈkeɪsii/) or Cruciferae (/kruːˈsɪfəri/)[2] is a medium-sized and economically important family of flowering plants commonly known as the mustards, the crucifers, or the cabbage family. Most are herbaceous plants, some shrubs, with simple, although sometimes deeply incised, alternatingly set leaves without stipules or in leaf rosettes, with terminal inflorescences without bracts, containing flowers with four free sepals, four free alternating petals, two short and four longer free stamens, and a fruit with seeds in rows, divided by a thin wall (or septum).

The family contains 372 genera and 4060 accepted species.[3] The largest genera are Draba (440 species), Erysimum (261 species), Lepidium (234 species), Cardamine (233 species), and Alyssum (207 species).

The family contains the cruciferous vegetables, including species such as Brassica oleracea (e.g., broccoli, cabbage, cauliflower, kale, collards), Brassica rapa (turnip, Chinese cabbage, etc.), Brassica napus (rapeseed, etc.), Raphanus sativus (common radish), Armoracia rusticana (horseradish), but also a cut-flower Matthiola (stock) and the model organism Arabidopsis thaliana (thale cress).

Pieris rapae and other butterflies of the family Pieridae are some of the best-known pests of Brassicaceae species planted as commercial crops. Trichoplusia ni (cabbage looper) moth is also becoming increasingly problematic for crucifers due to its resistance to commonly used pest control methods.[4] Some rarer Pieris butterflies, such as Pieris virginiensis, depend upon native mustards for their survival, in their native habitats. Some non-native mustards, such as garlic mustard, A. petiolata, an extremely invasive species in the United States, can be toxic to their larvae.

Taxonomy[edit]

Carl Linnaeus in 1753 regarded the Brassicaceae as a natural group, naming them "Klass" Tetradynamia. Alfred Barton Rendle placed the family in the order Rhoedales, while George Bentham and Joseph Dalton Hooker in their system published from 1862–1883, assigned it to their cohort Parietales (now the class Violales). Following Bentham and Hooker, John Hutchinson in 1948 and again in 1964 thought the Brassicaceae to stem from near the Papaveraceae. In 1994, a group of scientists including Walter Stephen Judd suggested to include the Capparaceae in the Brassicaceae. Early DNA-analysis showed that the Capparaceae - as defined at that moment - were paraphyletic, and it was suggested to assign the genera closest to the Brassicaceae to the Cleomaceae.[5] The Cleomaceae and Brassicaceae diverged approximately 41 million years ago.[6] All three families have consistently been placed in one order (variably called Capparales or Brassicales).[5] The APG II system, merged Cleomaceae and Brassicaceae. Other classifications have continued to recognize the Capparaceae, but with a more restricted circumscription, either including Cleome and its relatives in the Brassicaceae or recognizing them in the segregate family Cleomaceae. The APG III system has recently adopted this last solution, but this may change as a consensus arises on this point. Current insights in the relationships of the Brassicaceae, based on a 2012 DNA-analysis, are summarized in the following tree.[7][8]

core Brassicales
 
 
 
 
 

family Resedaceae

 
 
 

family Gyrostemonaceae

 
 
 

family Pentadiplandraceae

 
 
 
 

family Tovariaceae

 
 
 

family Capparaceae

 
 
 

family Cleomaceae

 
 

family Brassicaceae

 
 
 
 
 
 

family Emblingiaceae

 
 

Relationships within the family[edit]

Early classifications depended on morphological comparison only, but because of extensive convergent evolution, these do not provide a reliable phylogeny. Although a substantial effort was made through molecular phylogenetic studies, the relationships within the Brassicaceae have not always been well resolved yet. It has long been clear that the Aethionemae are sister of the remainder of the family.[9] One analysis from 2014 represented the relation between 39 tribes with the following tree.[10]

Brassicaceae
 

Aethionemae

 
 
 
 
 
 

Megacarpaeeae

 
 

Heliophileae

 
 
 
 

Coluteocarpeae

 
 

Conringieae

 
 
 
 
 

Buniadeae

 
 

Kernereae

 
 
 

Schizopetaleae

 
 
 
 

Thlaspideae

 
 
 
 
 

Isatieae

 
 

Sisymbrieae

 
 
 

Brassiceae

 
 

Thelypodieae

 
 
 

Eutremeae

 
 
 
 
 

Calepineae

 
 
 
 

Biscutelleae

 
 

Arabideae

 
 
 
 

Cochlearieae

 
 
 

Anchonieae

 
 
 
 
 

Hesperideae

 
 

Anastaticeae

 
 
 
 

Dontostemoneae

 
 

Chorisporeae

 
 
 
 

Euclidieae

 
 
 
 
 
 
 

Iberideae

 
 
 
 

Erysimeae

 
 
 
 
 
 

Lepidieae

 
 

Smelowskieae

 
 
 
 

Yinshanieae

 
 

Descurainieae

 
 
 
 
 

Camelinieae

 
 
 
 

Boechereae

 
 
 

Oreophytoneae

 
 

Halimolobeae

 
 
 
 
 

Physarieae

 
 

Crucihimalayeae

 
 
 
 
 
 

Cardamineae

 
 
 
 
 

Alysseae

 
 
 

Etymology and pronunciation[edit]

The name Brassicaceae comes to international scientific vocabulary from New Latin, from Brassica, the type genus, + -aceae,[11] a standardized suffix for plant family names in modern taxonomy. The genus name comes from the Classical Latin word brassica, referring to cabbage and other cruciferous vegetables. The alternative older name, Cruciferae, meaning "cross-bearing", describes the four petals of mustard flowers, which resemble a cross. Cruciferae is one of eight plant family names, not derived from a genus name and without the suffix -aceae that are authorized alternative names.[12]

Genera[edit]

Main article: List of Brassicaceae genera

Version 1 of the Plantlist website lists 349 genera.[13]

Description[edit]

Species belonging to the Brassicaceae are mostly annual, biennial, or perennial herbaceous plants, some are dwarf shrubs or shrubs, and very few vines. Although generally terrestrial, a few species such as water awlwort live submerged in fresh water. They may have a taproot or a sometimes woody caudex that may have few or many branches, some have thin or tuberous rhizomes, or rarely develop runners. Few species have multi-cellular glands. Hairs consist of one cell and occur in many forms: from simple to forked, star-, tree- or T-shaped, rarely taking the form of a shield or scale. They are never topped by a gland. The stems may be upright, rise up towards the tip, or lie flat, are mostly herbaceous but sometimes woody. Stems carry leaves or the stems may be leafless (in Caulanthus), and some species lack stems altogether. The leaves do not have stipules, but there may be a pair of glands at base of leafstalks and flowerstalks. The leaf may be seated or have a leafstalk. The leaf blade is usually simple, entire or dissected, rarely trifoliolate or pinnately compound. A leaf rosette at the base may be present or absent. The leaves along the stem are almost always alternately arranged, rarely apparently opposite.[14] The stomata are of the anisocytic type.[15] The genome size of Brassicaceae compared to that of other Angiosperm families is very small to small (less than 3.425 million base pairs per cell), varying from 150 Mbp in Arabidopsis thaliana and Sphaerocardamum spp., to 2375 Mbp Bunias orientalis. The number of homologous chromosome sets varies from four (n=4) in some Physaria and Stenopetalum species, five (n=5) in other Physaria and Stenopetalum species, Arabidopsis thaliana and a Mathiola species, to seventeen (n=17). About 35% of the species in which chromosomes have been counted have eight sets (n=8). Due to polyploidy, some species may have up to 256 individual chromosomes, with some very high counts in the North-American species of Cardamine, such as C. diphylla. Hybridisation is not unusual in Brassicaceae, especially in Arabis, Rorippa, Cardamine and Boechera. Hybridisation between species originating in Africa and California, and subsequent polyploidisation is surmised for Lepidium species native to Australia and New Zealand.[6]

Inflorescence and flower[edit]

Typical floral diagram of a Brassicaceae (Erysimum "Bowles' Mauve")

Flowers may be arranged in racemes, panicles, or corymbs, with pedicels sometimes in the axil of a bract, and few species have flowers that sit individually on flower stems that spring from the axils of rosette leaves. The orientation of the pedicels when fruits are ripe varies dependent on the species. The flowers are bisexual, star symmetrical (zygomorphic in Iberis and Teesdalia) and the ovary positioned above the other floral parts. Each flower has four free or seldomly merged sepals, the lateral two sometimes with a shallow spur, which are mostly shed after flowering, rarely persistent, may be reflexed, spreading, ascending, or erect, together forming a tube-, bell- or urn-shaped calyx. Each flower has four petals, set alternating with the sepals, although in some species these are rudimentary or absent. They may be differentiated into a blade and a claw or not, and consistently lack basal appendages. The blade is entire or has an indent at the tip, and may sometimes be much smaller than the claws. The mostly six stamens are set in two whorls: usually the two lateral, outer ones are shorter than the four inner stamens, but very rarely the stamens can all have the same length, and very rarely species have different numbers of stamens such as sixteen to twenty four in Megacarpaea, four in Cardamine hirsuta, and two in Coronopus. The filaments are slender and not fused, while the anthers consist of two pollen producing cavities, and open with longitudinal slits. The pollen grains are tricolpate. The receptacle carries a variable number of nectaries, but these are always present opposite the base of the lateral stamens.[14][7]

Ovary, fruit and seed[edit]

There is one superior pistil that consists of two carpels that may either sit directly above the base of the stamens or on a stalk. It initially consists of only one cavity but during its further development a thin wall grows that divides the cavity, both placentas and separates the two valves (a so-called false septum). Rarely, there is only one cavity without a septum. The 2–600 ovules are usually along the side margin of the carpels, or rarely at the top. Fruits are capsules that open with two valves, usually towards the top. These are called silique if at least three times longer than wide, or silicle if the length is less than three times the width. The fruit is very variable in its other traits. There may be one persistent style that connects the ovary to the globular or conical stigma, which is undivided or has two spreading or connivent lobes. The variously shaped seeds are usually yellow or brown in color, and arranged in one or two rows in each cavety. The seed leaves are entire or have a notch at the tip. The seed does not contain endosperm.[14]

Differences with similar families[edit]

Brassicaceae have a bisymmetical corolla (left is mirrored by right, stem-side by out-side, but each quarter is not symmetrical), a septum dividing the fruit, lack stipules and have simple (although sometimes deeply incised) leaves. The sister family Cleomaceae has bilateral symmetrical corollas (left is mirrored by right, but stem-side is different from out-side), stipules and mostly palmately divided leaves, but no septum.[14] Capparaceae generally have a gynophore, sometimes an androgynophore, and a variable number of stamens.[7]

Phytochemistry[edit]

Almost all Brassicaceae have C3 carbon fixation. The only exceptions are a few Moricandia species, which have a hybrid system between C3 and C4 carbon fixation, C4 fixation being more efficient in drought, high temperature and low nitrate availability.[16] Brassicaceae contain different cocktails of dozens of glucosinolates. They also contain enzymes called myrosinases, that convert the glucosinolates into isothiocyanates, thiocyanates and nitriles, which are toxic to many organisms, and so help guard against herbivory.[17]

Distribution[edit]

Brassicaceae can be found almost on the entire land surface of the planet, but it is absent from Antarctica, and in some areas in the tropics i.e. north-eastern Brazil, the Congo basin, Maritime Southeast Asia and tropical Australasia. The area of origin of the family is possibly the Irano-Turanian Region, where approximately 900 species occur in 150 different genera. About 530 of them are endemics. Next in abundance comes the Mediterranean Region with around 630 species (290 of which are endemic) in 113 genera. The family is less prominent in the Saharo-Arabian Region - 65 genera, 180 species of which 62 endemic - and North-America (comprising the North American Atlantic Region and the Rocky Mountain Floristic Region) - 99 genera, 780 species of which 600 endemic -. South-America has 40 genera containing 340 native species, Southern Africa 15 genera with over 100 species, and Australia and New-Zealand have 19 genera with 114 species between them.[6]

Ecology[edit]

Brassicaceae are almost exclusively pollinated by insects. A chemical mechanism in the pollen is active in many species to avoid selfing. Two notable exceptions are exclusive self pollination in closed flowers in Cardamine chenopodifolia, and wind pollination in Pringlea antiscorbutica.[7] Although it can be pollinated, Alliaria petiolata is self-fertile. Most species reproduce sexually through seed, but Cardamine bulbifera produces gemmae and in others, such as Cardamine pentaphyllos, the coral-like roots easily break into segments, that will grow into separate plants.[7] In some species, such as in the genus Cardamine, seed pods open with force and so catapult the seeds quite far. Many of these have sticky seed coats, assisting long distance dispersal by animals, and this may also explain several intercontinental dispersal events in the genus, and its near global distribution. Brassicaceae are common on serpentine and dolomite rich in magnesium. Over a hundred species in the family accumulate heavy metals, particularly zinc and nickel, which is a record percentage.[18] Several Alyssum species can accumulate nickel up to 0.3% of their dry weight, and may be useful in soil remediation or even bio-mining.[19]

Brassicaceae contain glucosinolates as well as myrosinases inside their cells. When the cell is damaged, the myrosinases hydrolise the glucosinolates, leading to the synthesis of isothiocyanates, which are compounds toxic to most animals, fungi and bacteria. Some insect herbivores have developed counter adaptations such as rapid absorption of the glucosinates, quick alternative breakdown into non-toxic compounds and avoiding cell damage. In the whites family (Pieridae), one counter mechanisme involves glucosinolate sulphatase, which changes the glucosinolate, so that it cannot be converted to isothiocyanate. A second is that the glucosinates are quickly broken down, forming nitriles.[17] Differences between the mixtures of glucosinolates between species and even within species is large, and individual plants may produce in excess of fifty individual substances. The energy penalty for synthesising all these glucosinolates may be as high as 15% of the total needed to produce a leaf. Bittercress (Barbarea vulgaris) also produces triterpenoid saponins. These adaptations and counter adaptations probably have led to extensive diversification in both the Brassicaceae and one of its major pests, the butterfly family Pieridae. A particular cocktail of volatile glucosinates triggers egg-laying in many species. Thus a particular crop can sometimes be protected by planting bittercress as a deadly bait, for the saponins kill the caterpillars, but the butterfly is still lured by the bittercress to lay its egg on the leaves.[20] A moth that feeds on a range of Brassicaceae is the diamondback moth (Plutella xylostella). Like the Pieridae, it is capable of converting isothiocyanates into less problematic nitriles. Managing this pest in crops became more complicated after resistance developed against a toxin produced by Bacillus thuringiensis, which is used as a wide spectrum biological plant protection against caterpillars. Parasitoid wasps that feed on such insect herbivores are attracted to the chemical compounds released by the plants, and thus are able to locate their prey. The cabbage aphid (Brevicoryne brassicae) stores glucosinolates and synthesises its own myrosinases, which may deter its potential predators.[18]

Since its introduction in the 19th century, Alliaria petiolata has been shown to be extremely successful as an invasive species in temperate North America due, in part, to its secretion of allelopathic chemicals. These inhibit the germination of most competing plants and kill beneficial soil fungi needed by many plants, such as many tree species, to successfully see their seedlings grow to maturity. The monoculture formation of an herb layer carpet by this plant has been shown to dramatically alter forests, making them wetter, having fewer and fewer trees, and having more vines such as poison ivy, Toxicodendron radicans. The overall herb layer biodiversity is also drastically reduced, particularly in terms of sedges and forbs. Research has found that removing 80 percent of the garlic mustard infestation plants did not lead to a particularly significant recovery of that diversity. Instead, it required around 100 percent removal. Given that not one of an estimated 76 species that prey on the plant has been approved for biological control in North America and the variety of mechanisms the plant has to ensure its dominance without them (e.g. high seed production, self-fertility, allelopathy, spring growth that occurs before nearly all native plants, roots that break easily when pulling attempts are made, a complete lack of palatability for herbivores at all life stages, et cetera) it is unlikely that such a high level of control can be established and maintained on the whole.[21][22][23][22][24][25][26] It is estimated that adequate control can be achieved with the introduction of two European weevils, including one that is monophagous.[27][28] However, the USDA's TAG group has blocked these introductions since 2004.[29] In addition to being invasive, garlic mustard also is a threat to native North American Pieris butterflies such as Pieris oleracea, as they preferentially oviposit on it, although it is toxic to their larvae.

Uses[edit]

Lunaria annua with dry walls of the fruit
Smelowskia americana is endemic to the midlatitude mountains of western North America.

This family includes important agricultural crops, among which many vegetables such as cabbage, broccoli, cauliflower, kale, Brussels sprouts, collard greens, Savoy, kohlrabi, and gai lan (Brassica oleracea), turnip, napa cabbage, bomdong, bok choy and rapini (Brassica rapa), rocket salad/arugula (Eruca sativa), garden cress (Lepidium sativum), watercress (Nasturtium officinale) and radish (Raphanus) and a few spices like horseradish (Armoracia rusticana), Brassica, wasabi (Eutrema japonicum), white, Indian and black mustard (Sinapis alba, Brassica juncea and B. nigra respectively). Vegetable oil is produced from the seeds of several species such as Brassica napus (rapeseed oil), perhaps providing the largest volume of vegetable oils of any species. Woad (Isatis tinctoria) was used in the past to produce a blue textile dye (indigo), but has largely been replaced by the same substance from unrelated tropical species like Indigofera tinctoria.[30]

Brassinosteroids are growing in agricultural and gardening importance.

The Brassicaceae also includes ornamentals, such as species of Aethionema, Alyssum, Arabis, Aubrieta, Aurinia, Cheiranthus, Erysimum, Hesperis, Iberis, Lobularia, Lunaria, Malcolmia, and Matthiola.[6] Honesty (Lunaria annua) is cultivated for the decorative value of the translucent remains of the fruits after drying.[31] However, it can be a pest species in areas where it is not native.

The small Eurasian weed Arabidopsis thaliana is widely used as model organism in the study of the molecular biology of flowering plants (Angiospermae).[32]

Some species are useful as food plants for Lepidoptera, such as certain wild mustard and cress species, such as Turritis glabra and Boechera laevigata that are utilized by several North American butterflies.[33] Garlic mustard, Alliaria petiolata, is one of the most aggressive and damaging invasive species in North America. Invasive aggressive mustard species are known for being self-fertile, seeding very heavily with small seeds that have a lengthy lifespan coupled with a very high rate of viability and germination, and for being completely unpalatable for both herbivores and insects in areas they are not native to. Garlic mustard is toxic to several rarer North American Pieris species.[24][34]

Main article: Cruciferous vegetables


Gallery[edit]

See also[edit]


References[edit]

  1. ^ Angiosperm Phylogeny Group (2009). "An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III" (PDF). Botanical Journal of the Linnean Society. 161 (2): 105–121. doi:10.1111/j.1095-8339.2009.00996.x. Retrieved 2013-07-06. 
  2. ^ Wikisource Chisholm, Hugh, ed. (1911). "Cruciferae". Encyclopædia Britannica. 7 (11th ed.). Cambridge University Press. p. 521. 
  3. ^ "Brassicaceae". The Plant List. 
  4. ^ Turini TA, Daugovish O, Koike ST, Natwick ET, Ploeg A, Dara SK, Fennimore SA, Joseph S, LeStrange M, Smith R, Subbarao KV, Westerdahl BB. Revised continuously. UC IPM Pest Management Guidelines Cole Crops. UC ANR Publication 3442. Oakland, CA.
  5. ^ a b Hall, J.C.; Sytsma, K.J.; Iltis, H.H. (2002). "Phylogeny of Capparaceae and Brassicaceae based on chloroplast sequence data". American Journal of Botany. 89 (11): 1826–1842. doi:10.3732/ajb.89.11.1826. PMID 21665611. 
  6. ^ a b c d Renate Schmidt, Ian Bancroft, eds. (2010). Genetics and Genomics of the Brassicaceae. Plant Genetics and Genomics: Crops and Models. 9. Springer Science & Business Media. 
  7. ^ a b c d e "Brassicaceae: Characters, Distribution and Types (With Diagram)". biologydiscussion. Retrieved 12 July 2017. 
  8. ^ Su, Jun-Xia; Wang, Wei; Zhang, Li-Bing; Chen, Zhi-Duan (June 2012). "Phylogenetic placement of two enigmatic genera, Borthwickia and Stixis, based on molecular and pollen data, and the description of a new family of Brassicales, Borthwickiaceae" (PDF). Taxon. 61 (3): 601–611. 
  9. ^ Al-Shehbaz, Ihsan A. (2012). "A generic and tribal synopsis of the Brassicaceae (Cruciferae)". Taxon. 61 (5): 931–954. 
  10. ^ Edger, Patrick P.; Tang, Michelle; Bird, Kevin A.; Mayfield, Dustin R.; Conant, Gavin; Mummenhoff, Klaus; Koch, Marcus A.; Pires, J. Chris (2014). "Secondary Structure Analyses of the Nuclear rRNA Internal Transcribed Spacers and Assessment of Its Phylogenetic Utility across the Brassicaceae (Mustards)". PLOS ONE. doi:10.1371/journal.pone.0101341. Retrieved 2017-07-11. 
  11. ^ Merriam-Webster, Merriam-Webster's Unabridged Dictionary, Merriam-Webster. 
  12. ^ "Article 18". ICBN. 
  13. ^ "Brassicaceae". The Plantlist. Retrieved 2017-10-09. 
  14. ^ a b c d Al-Shehbaz, I.A. (2012). "Neotropical Brassicaceae". Neotropikey - Interactive key and information resources for flowering plants of the Neotropics. Retrieved 2017-07-12. 
  15. ^ Metcalfe, C.R.; Chalk, L. (1950). Anatomy of Dicotyledons. 1: Leaves, Stem, and Wood in relation to Taxonomy, with notes on economic Uses. pp. 79–87. 
  16. ^ Naser A. Anjum, Iqbal Ahmad, M. Eduarda Pereira, Armando C. Duarte, Shahid Umar, Nafees A. Khan, eds. (2012). The Plant Family Brassicaceae: Contribution Towards Phytoremediation. Environmental Pollution. Springer Science & Business Media. 
  17. ^ a b Woods, Harry Arthur. Ecological and Environmental Physiology of Insects. Ecological and Environmental Physiology Series. 3. Oxford biological. 
  18. ^ a b "Brassicales". MOBOT. Retrieved 2017-07-18. 
  19. ^ Broadhurst, Catherine L.; Chaney, Rufus L. (2016). "Growth and Metal Accumulation of an Alyssum murale Nickel Hyperaccumulator Ecotype Co-cropped with Alyssum montanum and Perennial Ryegrass in Serpentine Soil". Frontiers in Plant Science. 7 (451). doi:10.3389/fpls.2016.00451. PMC 4824781 Freely accessible. PMID 27092164. 
  20. ^ Winde, I; Wittstock, U. (2011). "Insect herbivore counteradaptations to the plant glucosinolate-myrosinase system". Phytochemistry. 72 (13): 1566–75. doi:10.1016/j.phytochem.2011.01.016. PMID 21316065. 
  21. ^ Eubanks, HM.D., Hoffmann, J.H., Lewis, E.E., Liu, J., Melnick, R., Michaud, J.P., Ode, P., Pell, J.K., 2017. Biological Control Journal. Elsevier. https://www.journals.elsevier.com/Biological-Control
  22. ^ a b Becker, R., Gerber E., Hinz H., Katovich E., Panke B., Reardon R., Renz R., Van Riper L., 2013. Biology and Biological Control of Garlic Mustard. The Forest Technology Enterprise Team. https://www.fs.fed.us/foresthealth/technology/pdfs/FS_garlicmustard.pdf
  23. ^ UF IFAS, 2017. Biological Control. University of Florida. https://plants.ifas.ufl.edu/manage/control-methods/biological-control/
  24. ^ a b Driesche, F.V.; Blossey, B.; Hoodle, M.; Lyon, S.; Reardon, R., 2010. Biological Control of Invasive Plants in the Eastern United States. USDA Forest Service. Forest Health Technology Enterprise Team. http://wiki.bugwood.org/Archive:BCIPEUS
  25. ^ Davis, Adam. 2009. Munching on Garlic Mustard - A New Weevil in the Works. United States Department of Agriculture - AgResearch Magazine. https://agresearchmag.ars.usda.gov/2009/jul/weevil/
  26. ^ Blossy, B., Ode, P., Pell, J.K., 1999. Development of Biological Control for Garlic Mustard. Cornell University. https://www.dnr.illinois.gov/grants/documents/wpfgrantreports/1998l06w.pdf
  27. ^ Landis, Doug. "Management Options". Integrated Pest Management. Michigan State University. Retrieved 10 September 2017. 
  28. ^ Reardon, Richard. "FHTET Biological Control Program — Sponsored Projects" (PDF). FHTET Biological Control Program. USDA Forest Service. Retrieved 10 September 2017. 
  29. ^ Becker, R. (2017). "Implementing Biological Control of Garlic Mustard - Environment and Natural Resources Trust Fund 2017 RFP" (PDF). 
  30. ^ Guarino, Carmine; Casoria, Paolo; Menale, Bruno (2000). "Cultivation and use of isatis tinctoria L. (Brassicaceae) in Southern Italy". Economic Botany. 54 (3): 395–400. doi:10.1007/bf02864789. Retrieved 2017-08-12. 
  31. ^ Binney, Ruth (2012). The Gardener's Wise Words and Country Ways. David & Charles. ISBN 0715334239. 
  32. ^ Koornneef, Maarten; Meinke, David (2010). "The development of Arabidopsis as a model plant" (PDF). The Plant Journal. 61: 909–921. doi:10.1111/j.1365-313x.2009.04086.x. Retrieved 2017-08-12. 
  33. ^ Hilty, John (2017). "Smooth Rock Cress". Illinois Wildflowers. Dr. John Hilty. Retrieved 17 April 2018. 
  34. ^ Davis, S., 2015. Evaluating threats to the rare butterfly, Pieris virginiensis. Wright State University. https://etd.ohiolink.edu/!etd.send_file?accession=wright1431882480&disposition=inline
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