Rhopalosiphum maidis

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Rhopalosiphum maidis
Rhopalosiphum maidis from CSIRO.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hemiptera
Suborder: Sternorrhyncha
Family: Aphididae
Genus: Rhopalosiphum
Species:
R. maidis
Binomial name
Rhopalosiphum maidis
(Fitch, 1856) [1]
Synonyms

Rhopalosiphum maidis, common names corn leaf aphid and corn aphid, is an insect, and a pest of maize and other crops. It has a nearly worldwide distribution and is typically found in agricultural fields, grasslands, and forest-grassland zones. Among aphids that feed on maize, it is the most commonly encountered and most economically damaging, particularly in tropical and warmer temperate areas. In addition to maize, R. maidis damages rice, sorghum, and other cultivated and wild monocots. [2] [3] [4]

Contents

Description

The bodies of wingless parthenogenetic females are green or whitish-green. The head, antennae, legs, cornicles, tail, and transverse bands on the abdomen are black-brown. The body has sparse short hairs. The length of the antennae is less than half the length of the body. Cornicles are not longer than the finger-like tail. In winged females, the head and thoracic section are black-brown and the cornicles are shorter than in the wingless females. [2]

Most R. maidis populations are anholocyclic, i.e. reproduction occurs entirely by parthenogenesis. However, sexual reproduction has been reported in Pakistan and Korea, with Prunus ssp. as the primary host. [5] [6] In populations in Japan and Kenya, males but not sexually reproducing females have been found. [7] [8]

Agricultural interactions

In winter, winged parthenogenetic females and larvae survive on wild-growing monocots, from which they move to agricultural fields in the spring. Fields populate gradually, starting from the edges to the center. Reproduction is rapid, with up to twelve generations per year. The aphid population reaches a maximum late in the summer.

Dense populations of R. maidis on maize ( Zea mays ) can cause direct damage through the removal of photosynthates. [9] Large amounts of honeydew that is deposited by aphid feeding on maize tassels can prevent pollen shed and decrease yield by up to 90%. [10] [11] Several damaging maize viruses, including Maize yellow dwarf virus, Barley yellow dwarf virus , Sugarcane mosaic virus , and Cucumber mosaic virus , are transmitted by R. maidis.

In addition to feeding on maize, R. maidis infests a variety of cultivated grasses, including wheat, barley, oat, rye, sorghum, sugarcane, and rice. [2] [3] [4] Barley is a particularly suitable host for R. maidis, [12] though there also is considerable within-species variation in resistance. [13]

Chemical ecology

Rhopalosiphum maidis (corn leaf aphids) on Zea mays (maize) Corn leaf aphids (Rhopalosiphum maidis) on maize (Zea mays).jpg
Rhopalosiphum maidis (corn leaf aphids) on Zea mays (maize)

Under enhanced CO2 conditions, the growth rate and reproduction of R. maidis on barley were significantly decreased. [14] Volatiles of barley grown under enhanced CO2 were also less attractive than those from plants grown under atmospheric CO2. [15] Temperature and crowding have differential effects on wing formation in parthenogenetically reproducing R. maidis on barley. [16]

Maize inbred lines vary in their resistance to R. maidis and other insect pests. [17] Relative to other maize-feeding aphids ( Rhopalosiphum padi , Schizaphis graminum , Sitobion avenae , and Metopolophium dirhodum ), R. maidis exhibits a greater tolerance of benzoxazinoids, the most abundant class of maize defensive metabolites. [18] Nevertheless, lineage-specific variation in maize resistance to R. maidis was associated with differences in the abundance of 2,4-dihydroxy-7-methoxy-l,4-benzoxazin-3-one glucoside (DIMBOA-Glc), an abundant maize benzoxazinoid. [19] [20] [21] Both increased DIMBOA-Glc synthesis and reduced conversion to 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside (HDMBOA -Glc) can enhance maize seedling resistance to R. maidis. [19] [21] Maize mutations that knock out benzoxazinoid biosynthesis increase R. maidis reproduction. [21] [22] In some instances, caterpillar feeding can enhance the conversion of DIMBOA-Glc to HDMBOA-Glc, thereby increasing maize resistance against R. maidis. [23] The defense signaling molecules 2-oxo-phytodienoic acid (OPDA) and ethylene are involved in regulating maize resistance to R. maidis. [24] [25]

In olfactometer experiments, R. maidis were repelled by volatiles from damaged maize plants. [26] One of the major volatiles emitted by damaged maize is the terpene (E)‐β‐farnesene, which also functions as an alarm pheromone for aphids and thus may be repellent. Mutations of a maize terpene synthase, TPS2, made the plants more attractive for R. maidis. [22]

Genome sequencing

There is within-species variation in the chromosome numbers of R. maidis, with karyotypes of 2n = 8, 9, and 10 having been reported. Whereas R. maidis strains on maize tend to have 2n = 8, those on barley generally have 2n = 10. [27] [28] To better enable research related to ecological interactions, virus transmission, pesticide resistance, and other aspects of the species biology, a high-quality genome was assembled from a parthenogenetic R. maidis lineage collected from maize. [29] The assembled genome is 321 Mb in size and features a total of 17,629 protein-coding genes. Assembly of the genome was facilitated by the extremely low level of heterozygosity in the sequenced R. maidis isolate.

Hosts

Related Research Articles

<span class="mw-page-title-main">Aphid</span> Superfamily of insects

Aphids are small sap-sucking insects and members of the superfamily Aphidoidea. Common names include greenfly and blackfly, although individuals within a species can vary widely in color. The group includes the fluffy white woolly aphids. A typical life cycle involves flightless females giving live birth to female nymphs—who may also be already pregnant, an adaptation scientists call telescoping generations—without the involvement of males. Maturing rapidly, females breed profusely so that the number of these insects multiplies quickly. Winged females may develop later in the season, allowing the insects to colonize new plants. In temperate regions, a phase of sexual reproduction occurs in the autumn, with the insects often overwintering as eggs.

<span class="mw-page-title-main">Russian wheat aphid</span> Species of true bug

The Russian wheat aphid is an aphid that can cause significant losses in cereal crops. The species was introduced to the United States in 1986 and is considered an invasive species there. This aphid is pale green and up to 2 mm long. Cornicles are very short, rounded, and appear to be lacking. There is an appendage above the cauda giving the aphid the appearance of having two tails. The saliva of this aphid is toxic to the plant and causes whitish striping on cereal leaves. Feeding by this aphid will also cause the flag leaf to turn white and curl around the head causing incomplete head emergence. Its host plants are cereal grain crops including wheat and barley and to a lesser extent, wild grasses such as wheatgrasses, brome-grasses, ryegrasses and anything in the grass family.

<i>Maize dwarf mosaic virus</i> Species of plant pathogenic virus

Maize dwarf mosaic virus (MDMV) is a pathogenic plant virus of the family Potyviridae. Depending on the corn plant’s growth stage, the virus can have severe implications to the corn plant’s development which can also result in economic consequences to the producer of the crop.

Wheat yellow leaf virus (WYLV) is a wheat (Triticum spp. L.), barley (Hordeum vulgare L.), rye (Secale cereale M.Bieb.), and oat (Avena sativa L.) pathogenic virus of the family Closteroviridae. WYLV virions are 1600–1850 nm in length and 10 nm in diameter. The virus, like other members of its genus, is transmitted by aphids. Identified vectors include Rhopalosiphum padi L. and R. maidis Fitch. (Aphididae). The virus has been identified in crop plants in Japan, China, and Italy. Native host plants include Italian ryegrass (Festuca perennis Lam.) in Europe and Agropyron tsukushiense var. transiens Ohwi in Japan. The virus proliferates in the phloem of its host plants, interfering with the plant's ability to produce sufficient chlorophyll (Chlorosis), causing the leaves to yellow and the plant to die.

<i>Soybean mosaic virus</i> Plant disease

Soybean mosaic virus (SMV) is a member of the plant virus genus Potyvirus. It infects mainly plants belonging to the family Fabaceae but has also been found infecting other economically important crops. SMV is the cause of soybean mosaic disease that occurs in all the soybean production areas of the world. Soybean is one of the most important sources of edible oil and proteins and pathogenic infections are responsible for annual yield losses of about $4 billion in the United States. Among these pathogens, SMV is the most important and prevalent viral pathogen in soybean production worldwide. It causes yield reductions of about 8% to 35%, but losses as high as 94% have been reported.

<span class="mw-page-title-main">DIMBOA</span> Chemical compound

DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one) is a naturally occurring hydroxamic acid, a benzoxazinoid. DIMBOA is a powerful antibiotic present in maize, wheat, rye, and related grasses,

<i>Rhopalosiphum</i> Genus of true bugs

Rhopalosiphum is a genus of aphid of the family Aphididae that includes 16 species worldwide. Apart from sucking the phloem of host plants and thereby being treated in agriculture as pests, some species are vectors for viral pathogens.

<span class="mw-page-title-main">Soybean aphid</span> Species of true bug

The soybean aphid is an insect pest of soybean that is exotic to North America. The soybean aphid is native to Asia. It has been described as a common pest of soybeans in China and as an occasional pest of soybeans in Indonesia, Japan, Korea, Malaysia, the Philippines, and Thailand. The soybean aphid was first documented in North America in Wisconsin in July 2000. Ragsdale et al. (2004) noted that the soybean aphid probably arrived in North America earlier than 2000, but remained undetected for a period of time. Venette and Ragsdale (2004) suggested that Japan probably served as the point of origin for the soybean aphid's North American invasion. By 2003, the soybean aphid had been documented in Delaware, Georgia, Illinois, Indiana, Iowa, Kansas, Kentucky, Michigan, Minnesota, Mississippi, Missouri, Nebraska, New York, North Dakota, Ohio, Pennsylvania, South Dakota, Virginia, West Virginia, and Wisconsin. Together, these states accounted for 89% of the 63,600,000 acres (257,000 km2) of soybean planted in the United States in 2007.

<i>Myzus persicae</i> Aphid of peach, potato, other crops

Myzus persicae, known as the green peach aphid, greenfly, or the peach-potato aphid, is a small green aphid belonging to the order Hemiptera. It is the most significant aphid pest of peach trees, causing decreased growth, shrivelling of the leaves and the death of various tissues. It also acts as a vector for the transport of plant viruses such as cucumber mosaic virus (CMV), potato virus Y (PVY) and tobacco etch virus (TEV). Potato virus Y and potato leafroll virus can be passed to members of the nightshade/potato family (Solanaceae), and various mosaic viruses to many other food crops.

<i>Peregrinus maidis</i> Species of true bug

Peregrinus maidis, commonly known as the corn planthopper, is a species of insect in the order Hemiptera and the family Delphacidae. It is widespread throughout most tropical and subtropical regions on earth, including southern North America, South America, Africa, Australia, Southeast Asia and China. P. maidis are a commercially important pest of maize and its relatives. In addition to physical plant damage, P. maidis is the vector for several species-specific maize viruses, including maize stripe virus, maize mosaic virus and the non-pathogenic Peregrinus maidis reovirus.

2,4-dihydroxy-1,4-benzoxazin-3-one-glucoside dioxygenase (EC 1.14.20.2, BX6 (gene), DIBOA-Glc dioxygenase) is an enzyme with systematic name (2R)-4-hydroxy-3-oxo-3,4-dihydro-2H-1,4-benzoxazin-2-yl beta-D-glucopyranoside:oxygen oxidoreductase (7-hydroxylating). This enzyme catalyses the following chemical reaction

Function Maize gene for first step in biosynthesis of benzoxazin, which aids in resistance to insect pests, pathogenic fungi and bacteria.

<i>Aphis craccivora</i> Species of true bug

Aphis craccivora, variously known as the cowpea aphid, groundnut aphid or black legume aphid, is a true bug in the family Aphididae. Originally of probable Palearctic origin, it is now an invasive species of cosmopolitan distribution.

<i>Melanaphis sacchari</i> Species of insect

The sugarcane aphid,, is an aphid in the superfamily Aphidoidea in the order Hemiptera. It is a true bug and sucks sap from plants. It is mostly found in Saccharum and Sorghum species. The species primarily reproduces via parthenogenesis, although sexual morphs have been discovered in China, Japan, and Mexico - in China the eggs overwinter in the host Miscanthus sacchariflorus.

<i>Rhopalosiphum padi</i> Species of true bug

Bird cherry-oat aphid is an aphid in the superfamily Aphidoidea in the order Hemiptera. It is a true bug and sucks sap from plants. It is considered a major pest in cereal crops, especially in temperate regions, as well as other hosts in parts of Northern Europe. It is the principal vector of many viruses in economically important field crops.

<i>Rhopalosiphum rufiabdominale</i> Species of aphid

Rhopalosiphum rufiabdominale, the rice root aphid or red rice root aphid, is a sap-sucking insect pest with a wide host range and a global distribution. As a member of the superfamily Aphidoidea, it is one of 16 species of the genus Rhopalosiphum. Adults and nymphs are soft-bodied and usually dark green with brown, red, or yellow tones. Like all aphids, reproduction is sexual and asexual, depending on the environmental conditions and host plant. Rice root aphids cause injury to external plant parts, namely the roots or stem, by feeding on plant sap and vector several important plant viruses. The hosts of this pest extend across multiple plant families with most belonging to Rosaceae, Poaceae, and Solanaceae. R. rufiabdominale is universally associated with Prunus species but also infests various field crops, greenhouse vegetables, cannabis, and other ornamental plants. While this aphid originates from east Asia, it spans nearly every continent. Dispersal is particularly widespread across the United States, India, and Australia, with crop damage documented in multiple instances, although economic losses are primarily associated with Japanese rice crops. Nonetheless, it remains a pest of serious concern due to its high mobility, discrete habitat, and adaptive plasticity, giving it the rightful reputation as a successful invader.

<i>Schizaphis graminum</i> Species of true bug

The greenbug, or wheat aphid, is an aphid in the superfamily Aphidoidea in the order Hemiptera. It is a true bug and feeds on the leaves of Gramineae (grass) family members.

<span class="mw-page-title-main">Corn stunt disease</span> Bacterial plant disease

Corn stunt disease is a bacterial disease of corn and other grasses. Symptoms include stunted growth and leaves turning red. It is caused by the bacterium Spiroplasma kunkelii.

<span class="mw-page-title-main">Georg Jander</span> American plant biologist

Georg Jander is an American plant biologist at the Boyce Thompson Institute in Ithaca, New York. He has an adjunct appointment in the Plant Biology Section of the School of Integrative Plant Sciences at Cornell University. Jander is known for his molecular research identifying genes for biochemical compounds of ecological and agricultural importance, particularly those plant traits involved in resistance to insect pests.

References

  1. ↑ Fauna Europaea
  2. 1 2 3 Blackman, Roger L.; Eastop, Victor Frank (2000). Aphids on the world's crops : an identification and information guide (2nd ed.). Chichester, West Sussex, England: Wiley. ISBN   0471851914. OCLC   42290200.
  3. 1 2 "Rhopalosiphum maidis (Fitch) - Maize Aphid". Ethiopia.ipm-info.org. 2008-05-03. Retrieved 2011-08-29.
  4. 1 2 "Rhopalosiphum maidis". Extento.hawaii.edu. Retrieved 2011-08-29.
  5. ↑ Lee, S; Holman, J; Havelka, J (2002). Illustrated Catalogue of Aphididae in the Korean Peninsula Part I, Subfamily Aphidinae. Korea Research Institute of Bioscience and Biotechnology.
  6. ↑ Remaudière, G (1991). "Découverte au Pakistan de l'hôte primaire de Rhopalosiphum maidis". C R Acad Agric Fr. 77: 61–62.
  7. ↑ Eastop, V. F. (2009). "The Males of Rhopalosiphum Maidis (Fitch) and a Discussion on the Use of Males in Aphid Taxonomy". Proceedings of the Royal Entomological Society of London, Series A. 29 (4–6): 84–85. doi:10.1111/j.1365-3032.1954.tb01204.x. ISSN   0375-0418.
  8. ↑ Torikura, H (1991). "Revisional notes on Japanese Rhopalosiphum, with keys to species based on the morphs on the primary host". Japanese Journal of Entomology. 59: 257–273.
  9. ↑ Bing, J. W.; Guthrie, W. D.; Dicke, F. F.; Obrycki, J. J. (1991). "Seedling Stage Feeding by Corn Leaf Aphid (Homoptera: Aphididae): Influence on Plant Development in Maize". Journal of Economic Entomology. 84 (2): 625–632. doi:10.1093/jee/84.2.625. ISSN   1938-291X.
  10. ↑ Foott, W. H.; Timmins, P. R. (1973). "Effects of Infestations by the Corn Leaf Aphid, Rhopalosiphum Maidis (Homoptera: Aphididae), on Field Corn in Southwestern Ontario". The Canadian Entomologist. 105 (3): 449–458. doi:10.4039/ent105449-3. ISSN   0008-347X. S2CID   84422311.
  11. ↑ Cerena, MJ; Glogoza, P (2004). "Resistance of maize to the corn leaf aphid: A review". Maydica. 49: 241–254.
  12. ↑ El‐Ibrashy, M. T.; El‐Ziady, Samira; Riad, Aida A. (1972). "Laboratory Studies on the Biology of the Corn Leaf Aphid, Rhopalosiphum Maidis (homoptera: Aphididae)". Entomologia Experimentalis et Applicata. 15 (2): 166–174. doi:10.1111/j.1570-7458.1972.tb00192.x. ISSN   1570-7458. S2CID   85324421.
  13. ↑ Gill, C. C.; Metcalfe, D. R. (1977). "Resistance in barley to the corn leaf aphid rhopalosiphum maidis". Canadian Journal of Plant Science. 57 (4): 1063–1070. doi:10.4141/cjps77-158. ISSN   0008-4220.
  14. ↑ Chen, Yu; Serteyn, Laurent; Wang, Zhenying; He, KangLai; Francis, Frederic (2019). "Reduction of Plant Suitability for Corn Leaf Aphid (Hemiptera: Aphididae) Under Elevated Carbon Dioxide Condition". Environmental Entomology. 48 (4): 935–944. doi:10.1093/ee/nvz045. hdl:2268/237585. ISSN   0046-225X. PMID   31116399. S2CID   162171362.
  15. ↑ Chen, Yu; Martin, Clément; Fingu Mabola, Junior Corneille; Verheggen, François; Wang, Zhenying; He, KangLai; Francis, Frederic (2019). "Effects of Host Plants Reared under Elevated CO2 Concentrations on the Foraging Behavior of Different Stages of Corn Leaf Aphids Rhopalosiphum maidis". Insects. 10 (6): 182. doi: 10.3390/insects10060182 . ISSN   2075-4450. PMC   6628410 . PMID   31234573.
  16. ↑ Chen, Yu; Verheggen, François J.; Sun, Dandan; Wang, Zhenying; Francis, Frederic; He, KangLai (2019). "Differential wing polyphenism adaptation across life stages under extreme high temperatures in corn leaf aphid". Scientific Reports. 9 (1): 8744. Bibcode:2019NatSR...9.8744C. doi:10.1038/s41598-019-45045-x. ISSN   2045-2322. PMC   6584643 . PMID   31217431.
  17. ↑ Meihls, L. N.; Kaur, H.; Jander, G. (2012). "Natural Variation in Maize Defense against Insect Herbivores". Cold Spring Harbor Symposia on Quantitative Biology. 77: 269–283. doi: 10.1101/sqb.2012.77.014662 . ISSN   0091-7451. PMID   23223408.
  18. ↑ Caballero, Paula P.; Ramírez, Claudio C.; Niemeyer, Hermann M. (2001). "Specialisation pattern of the aphid Rhopalosiphum maidis is not modified by experience on a novel host". Entomologia Experimentalis et Applicata. 100 (1): 43–52. doi:10.1046/j.1570-7458.2001.00846.x. ISSN   1570-7458. S2CID   85808381.
  19. 1 2 Meihls, L. N.; Handrick, V.; Glauser, G.; Barbier, H.; Kaur, H.; Haribal, M. M.; Lipka, A. E.; Gershenzon, J.; Buckler, E. S. (2013). "Natural Variation in Maize Aphid Resistance Is Associated with 2,4-Dihydroxy-7-Methoxy-1,4-Benzoxazin-3-One Glucoside Methyltransferase Activity". The Plant Cell. 25 (6): 2341–2355. doi:10.1105/tpc.113.112409. ISSN   1040-4651. PMC   3723630 . PMID   23898034.
  20. ↑ Mijares, Valeria; Meihls, Lisa; Jander, Georg; Tzin, Vered (2013). "Near-isogenic lines for measuring phenotypic effects of DIMBOA-Glc methyltransferase activity in maize". Plant Signaling & Behavior. 8 (10): e26779. doi:10.4161/psb.26779. ISSN   1559-2324. PMC   4091059 . PMID   24494232.
  21. 1 2 3 Betsiashvili, M.; Ahern, K. R.; Jander, G. (2015). "Additive effects of two quantitative trait loci that confer Rhopalosiphum maidis (corn leaf aphid) resistance in maize inbred line Mo17". Journal of Experimental Botany. 66 (2): 571–578. doi:10.1093/jxb/eru379. ISSN   0022-0957. PMC   4286405 . PMID   25249072.
  22. 1 2 Tzin, Vered; Fernandez-Pozo, Noe; Richter, Annett; Schmelz, Eric A; Schoettner, Matthias; Schäfer, Martin; Ahern, Kevin R; Meihls, Lisa N; Kaur, Harleen (2015). "Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays". Plant Physiology. 169 (3): 1727–43. doi:10.1104/pp.15.01039. ISSN   0032-0889. PMC   4634079 . PMID   26378100.
  23. ↑ Tzin, Vered; Lindsay, Penelope L.; Christensen, Shawn A.; Meihls, Lisa N.; Blue, Levi B.; Jander, Georg (2015). "Genetic mapping shows intraspecific variation and transgressive segregation for caterpillar-induced aphid resistance in maize". Molecular Ecology. 24 (22): 5739–5750. doi:10.1111/mec.13418. PMID   26462033. S2CID   206182798.
  24. ↑ Varsani, Suresh; Grover, Sajjan; Zhou, Shaoqun; Koch, Kyle G.; Huang, Pei-Cheng; Kolomiets, Michael V.; Williams, W. Paul; Heng-Moss, Tiffany; Sarath, Gautam (2019). "12-Oxo-Phytodienoic Acid Acts as a Regulator of Maize Defense against Corn Leaf Aphid". Plant Physiology. 179 (4): 1402–1415. doi:10.1104/pp.18.01472. ISSN   0032-0889. PMC   6446797 . PMID   30643012.
  25. ↑ Louis, Joe; Basu, Saumik; Varsani, Suresh; Castano-Duque, Lina; Jiang, Victoria; Williams, W. Paul; Felton, Gary W.; Luthe, Dawn S. (2015). "Ethylene Contributes to maize insect resistance1 -Mediated Maize Defense against the Phloem Sap-Sucking Corn Leaf Aphid". Plant Physiology. 169 (1): 313–324. doi:10.1104/pp.15.00958. ISSN   0032-0889. PMC   4577432 . PMID   26253737.
  26. ↑ Bernasconi, Marco L.; Turlings, Ted C. J.; Ambrosetti, Lara; Bassetti, Paolo; Dorn, Silvia (1998). "Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis". Entomologia Experimentalis et Applicata. 87 (2): 133–142. doi:10.1046/j.1570-7458.1998.00315.x. ISSN   1570-7458. S2CID   86187075.
  27. ↑ Blackman, R. L.; Brown, P. A. (1988). "Karyotype variation in the corn leaf aphid, Rhopalosiphum maidis (Fitch), species complex (Hemiptera: Aphididae) in relation to host-plant and morphology". Bulletin of Entomological Research. 78 (2): 351–363. doi:10.1017/S0007485300013110. ISSN   1475-2670.
  28. ↑ Blackman, RA; Brown, PA (1991). "Morphometric variation within and between populations of Rhopalosiphum maidis with a discussion of the taxonomic treatment of permanently parthenogenetic aphids (Homoptera: Aphididae)". Entomologia Generalis. 16 (2): 97–113. doi:10.1127/entom.gen/16/1991/097.
  29. ↑ Chen W, Shakir S, Bigham M, Richter A, Fei Z, Jander G (April 2019). "Genome sequence of the corn leaf aphid (Rhopalosiphum maidis Fitch)". GigaScience. 8 (4). doi:10.1093/gigascience/giz033. PMC   6451198 . PMID   30953568. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
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