One of the genes responsible for producing different "morphs" of primrose flowers has been identified

Barrett

Charlesworth

Charnov

Darwin

Lloyd

Ohnishi

Renner

eLife

PubMed

Pannell, J.R.

Cossard, G.

Serveur académique lausannois

PLANT REPRODUCTIONLong story shortOne of the genes responsible for producing different "morphs" ofprimrose flowers has been identified.JOHN R PANNELL AND GUILLAUME COSSARDThe vast majority of flowering plants arehermaphrodites, with both male andfemale parts in each of their flowers(Renner, 2014). This strategy is clearly a suc-cessful one, coming with several likely advan-tages including that, by producing both pollenand ovules, each flower has more opportunitiesto pass genes on to the next generation(Charnov et al., 1976). Although hermaphro-dites might also benefit from the possibility ofself-fertilization (and many do), mosthermaphrodites do all they can to avoid ‘selfing’because it is often detrimental to a plant’s fit-ness (Charlesworth and Willis, 2009; Bar-rett, 2002). Hermaphroditic plants have thusevolved a wonderful array of mechanisms thathelp them to promote outcrossing.One of these mechanisms, known as hetero-styly, involves male and female parts of the flower(the stamen and the stigma) being in differentplaces in different flowers. The stigma sits on theend of a stalk called the style. Some flowers havelong styles and hold their stamens, which pro-duce pollen, deep in the floral tube, whereasothers have short styles and hold their stamensmuch higher in the floral tube (Figure 1A). Thismeans that pollen from a long-styled plant ismore likely to pollinate a short-styled flower, andvice versa. Long- and short-styled plants may alsodiffer in the size and colour of their pollen grainsand the texture of their stigmas, and outcrossingis only possible between different morphs (Bar-rett, 2002). Remarkably, despite its complexity,heterostyly has evolved repeatedly in floweringplants and is found in at least 30 families, includ-ing the primroses (genus Primula).Charles Darwin was fascinated by heterostyly(Darwin, 1877) and we now know that it iscaused by the expression of several genes thatare inherited together as a single genetic unit(locus). However, working out how these genesinfluence the development of flowers has beensomething of a holy grail in the field. Now, ineLife, Michael Lenhard at the University of Pots-dam and colleagues – including Cuong NguyenHuu as first author – have identified the genethat is responsible for the different lengths ofstyles in primroses, and shown how it works(Huu et al., 2016).Huu et al. found that a gene calledCYP734A50 is only present in short-styled flow-ers in several species of primrose, and esti-mates of transcript read coverage suggest thatonly one copy of the gene is present in theseflowers. CYP734A50 encodes an enzyme thatdegrades plant hormones called brassinoste-roids, which are known to promote cell elonga-tion (Ohnishi et al., 2006). Huu et al. foundthat a particular brassinosteroid, castasterone,is present at higher levels in long styles than inshort styles, and that treating short styleswith another brassinosteroid increased stylelength (Figure 1B). Moreover, virus-inducedsilencing of CYP734A50 in young plants withCopyright Pannell and Cossard.This article is distributed under theterms of the Creative CommonsAttribution License, which permitsunrestricted use and redistributionprovided that the original author andsource are credited.Related research article Huu CN, Kappel C,Keller B, Sicard A, Takebayashi Y,Breuninger H, Nowak MD, Ba¨urle I,Himmelbach A, Burkart M, Ebbing-Lohaus T,Sakakibara H, Altschmied L, Conti E,Lenhard M. 2016. Presence versus absenceof CYP734A50 underlies the style-lengthdimorphism in primroses. eLife 5:e17956.doi: 10.7554/eLife.17956Pannell and Cossard. eLife 2016;5:e20314. DOI: 10.7554/eLife.20314 1 of 3INSIGHTshort styles resulted in the production of flow-ers with longer styles.It has been thought for a long time, based ontheoretical reasoning and comparative analysis,that the first mutation in the evolution of hetero-styly was a mutation that reduced style length,and that the expression of this mutated geneshould be dominant over the expression of itshomologous gene at the style-length locus(Lloyd and Webb, 1992a; 1992b). The resultsof Huu et al. are consistent with the idea thatthe expression of the CYP734A50 gene in short-styled individuals is genetically dominant. Buthow did this dominance come about?Huu et al. show that CYP734A50 is the resultof the duplication of a gene that degrades bras-sinosteroids more generally. The duplicationevent occurred early in the evolution of the Prim-ula genus, and the duplicated copy then evolvedto be expressed only in styles. The presence orabsence of the duplication has been maintainedin the genus by a process called negativeFigure 1. Heterostyly in primroses. (A) Schematic diagrams of a long-styled (left) and short-styled flower (right)from a distylous species such as Primula vulgaris. When an insect enters a long-styled flower it would pick uppollen mainly on its head. If this insect then visits a short-styled flower, the stigma would pick up the pollen fromthe insect’s head. Meanwhile, the high stamens would deposit fresh pollen on to the insect’s abdomen foreffective transfer to the stigmas of long-styled flowers. (B) Huu et al. identified CYP730A50 as a duplicated genethat alters style length in Primula flowers. Flowers without CYP730A50 (left) produce brassinosteroids, which causethe cells in the style to elongate and produce a long style. On the other hand, flowers with this gene (right) in theS-locus suppress the production of brassinosteroids, which leads to a short style.Pannell and Cossard. eLife 2016;5:e20314. DOI: 10.7554/eLife.20314 2 of 3Insight Plant reproduction Long story shortfrequency-dependent selection, whereby the fit-ness of a trait (e.g. short styles) increases if itbecomes rare, thus preventing its loss.In his short autobiography, Darwin reflectedthat "I do not think anything in my scientific lifehas given me so much satisfaction as making outthe meaning of the structure of heterostylousflowers". Like so much of his work, the hypothe-sis that he put forward has stood the test oftime and remains the favoured explanation forhow and why heterostyly evolved (Bar-rett, 2002). By identifying the gene that controlsstyle length, the work of Huu et al. is an impor-tant step towards understanding the underlyingmechanisms involved in heterostyly. A futurechallenge is to understand the evolutionary his-tory of the other genes involved in heterostylyand to work out what roles they play in flowerdevelopment.John R Pannell is in the Department of Ecologyand Evolution, University of Lausanne, Lausanne,SwitzerlandJohn.Pannell@unil.chGuillaume Cossard is in the Department ofEcology and Evolution, University of Lausanne,Lausanne, Switzerlandhttp://orcid.org/0000-0003-4633-5159Competing interests: The authors declare thatno competing interests exist.Published 06 September 2016ReferencesBarrett SC. 2002. Sexual interference of the floralkind. Heredity 88:154–159. doi: 10.1038/sj.hdy.6800020Charlesworth D, Willis JH. 2009. The genetics ofinbreeding depression. Nature Reviews Genetics 10:783–796. doi: 10.1038/nrg2664Charnov EL, Smith JM, Bull JJ. 1976. Why be anhermaphrodite? Nature 263:125–126. doi: 10.1038/263125a0Darwin C. 1877. The Different Forms of Flowers onPlants of the Same Species. New York: Appleton . doi:10.5962/bhl.title.46988Huu CN, Kappel C, Keller B, Sicard A, Takebayashi Y,Breuninger H, Nowak MD, Ba¨urle I, Himmelbach A,Burkart M, Ebbing-Lohaus T, Sakakibara H, AltschmiedL, Conti E, Lenhard M. 2016. Presence versus absenceof CYP734A50 underlies the style-length dimorphismin primroses. eLife 5:17956. doi: 10.7554/eLife.17956Lloyd DG, Webb CJ. 1992a. The evolution ofheterostyly. In: Barrett SCH (Ed). Evolution andFunction of Heterostyly. Berlin: Springer Verlag. p.151–178. doi: 10.1007/978-3-642-86656-2_6Lloyd DG, Webb CJ. 1992b. The selection ofheterostyly. In: Barrett SCH (Ed). Evolution andFunction of Heterostyly. Berlin: Springer Verlag. p.179–207. doi: 10.1007/978-3-642-86656-2_7Ohnishi T, Szatmari AM, Watanabe B, Fujita S, BancosS, Koncz C, Lafos M, Shibata K, Yokota T, Sakata K,Szekeres M, Mizutani M. 2006. C-23 hydroxylation byArabidopsis CYP90C1 and CYP90D1 reveals a novelshortcut in brassinosteroid biosynthesis. The Plant Cell18:3275–3288. doi: 10.1105/tpc.106.045443Renner SS. 2014. The relative and absolutefrequencies of angiosperm sexual systems: dioecy,monoecy, gynodioecy, and an updated onlinedatabase. American Journal of Botany 101:1588–1596.doi: 10.3732/ajb.1400196Pannell and Cossard. eLife 2016;5:e20314. DOI: 10.7554/eLife.20314 3 of 3Insight Plant reproduction Long story short

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One of the genes responsible for producing different "morphs" of primrose flowers has been identified.</jats:p

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