A knot of hybrids: Differentiating Asian knotweeds in North-Eastern France using genetic, cytological, and morphological data

Enzo Jugieau , Victor Talmot , Cybill Staentzel , Sandra Noir , Laurent Hardion

Journal of Systematics and Evolution ›› 2024, Vol. 62 ›› Issue (6) : 1218 -1226.

PDF
Journal of Systematics and Evolution ›› 2024, Vol. 62 ›› Issue (6) : 1218 -1226. DOI: 10.1002/jse.13075
Research Article

A knot of hybrids: Differentiating Asian knotweeds in North-Eastern France using genetic, cytological, and morphological data

Author information +
History +
PDF

Abstract

The two invasive Reynoutria species,Reynoutria japonica var. japonica and Reynoutria sachalinensis, and their hybrid Reynoutria x bohemica are often misidentified by managers and nonspecialists. The taxonomic confusions are all the more exacerbated by the infraspecific variability of introduced populations in terms of morphology, genetic diversity, and ploidy level. We resolved the identity of North-Eastern French invasive populations using 4582 single-nucleotide polymorphisms (SNPs) from a RADseq analysis, DNA contents estimated by flow cytometry, and 12 vegetative morphometric variables. The SNPs supported only one single genotype for R. japonica over 11 localities, while the nine localities of Reynoutria x bohemica were represented by one genotype each. Estimation of genome size using DAPI staining and flow cytometry revealed only octoploid cytotypes for R. japonica and hexaploid cytotypes for R. x bohemica, whereas R. sachalinensis was represented by tetraploid and hexaploid cytotypes. Among morphometric variables, no single one allows for a clear differentiation of the three taxa. We propose a combination of characters to easily and quickly identify these three invasive taxa based on six vegetative criteria including leaf and apex length, as well as leaf shape, leaf base, and apex shape, and the extrafloral nectaries on the node.

Keywords

Fallopia spp / flow cytometry / invasive plant species / morphometric analysis / population genetics / RADseq / Reynoutria spp

Cite this article

Download citation ▾
Enzo Jugieau, Victor Talmot, Cybill Staentzel, Sandra Noir, Laurent Hardion. A knot of hybrids: Differentiating Asian knotweeds in North-Eastern France using genetic, cytological, and morphological data. Journal of Systematics and Evolution, 2024, 62(6): 1218-1226 DOI:10.1002/jse.13075

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

AbgrallC,ForeyE, MignotL,Chauvat M. 2018. Invasion by Fallopia japonica alters soil food webs through secondary metabolites. Soil Biology and Biochemistry 127:100–109.

[2]

AguileraAG,AlpertP, DukesJS,Harrington R. 2010. Impacts of the invasive plant Fallopia japonica (Houtt.) on plant communities and ecosystem processes. Biological Invasions 12(5):1243–1252.

[3]

BaileyJ,Wisskirchen R. 2004. The distribution and origins of Faúopia × bohemica (Polygonaceae) in Europe. Nordic Journal of Botany 24(2):173–199.

[4]

BaileyJP,Bímová K,MandákB. 2009. Asexual spread versus sexual reproduction and evolution in Japanese Knotweed s.l. sets the stage for the “Battle of the Clones”. Biological Invasions 11(5):1189–1203.

[5]

BeerlingDJ,BaileyJP, ConollyAP. 1994. Fallopia japonica (Houtt.) Ronse Decraene. The Journal of Ecology 82(4):959–979.

[6]

BímováK. 2003. Experimental study of vegetative regeneration in four invasive Reynoutria taxa (Polygonaceae). Plant Ecology 166(1):1–11.

[7]

BímováK,Mandák B,KašparováI. 2004. How does Reynoutria invasion fit the various theories of invasibility? Journal of Vegetation Science 15(4):495–504.

[8]

BougeardS,DrayS. 2018. Supervised multiblock analysis in R with the ade4 package. Journal of Statistical Software 86(1):1–17.

[9]

BramMR,McNairJN. 2004. Seed germinability and its seasonal onset of Japanese knotweed (Polygonum cuspidatum). Weed Science 52(5):759–767.

[10]

BzdegaK,JaniakA, KsiążczykT,LewandowskaA,Gancarek M,SliwinskaE,Tokarska-GuzikB. 2016. A survey of genetic variation and genome evolution within the invasive Fallopia complex. PLoS One 11(8):e0161854.

[11]

ColleranB,LacySN, RetamalMR. 2020. Invasive Japanese knotweed (Reynoutria japonica Houtt.) and related knotweeds as catalysts for streambank erosion. River Research and Applications 36(9):1962–1969.

[12]

DavidsonAM,Jennions M,NicotraAB. 2011. Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis: Invasive species have higher phenotypic plasticity. Ecology Letters 14(4):419–431.

[13]

DesjardinsSD,PashleyCH, BaileyJP. 2023. A taxonomic, cytological and genetic survey of Japanese knotweed s.l. in New Zealand indicates multiple secondary introductions from Europe and a direct introduction from Japan. New Zealand Journal of Botany 61(1):49–66.

[14]

DeWoodyJ,RoweCA, HipkinsVD,Mock KE. 2008. “Pando” lives: Molecular genetic evidence of a giant aspen clone in central Utah. Western North American Naturalist 68(4):493–497.

[15]

DiagneC,LeroyB, VaissièreAC,GozlanRE,RoizD, JarićI,SallesJM,Bradshaw CJA,CourchampF. 2021. High and rising economic costs of biological invasions worldwide. Nature 592(7855):571–576.

[16]

DommangetF,EvetteA, PiolaF,Thiébaut M,MartinFM,RouifedS,Dutartre A,SaratE,LavoieC,CottetM. 2019. Les renouées asiatiques, espèces exotiques envahissantes. Sciences Eaux & Territoires 27:8–13.

[17]

DoyleJJ,DoyleJL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15.

[18]

EatonDAR,Overcast I. 2020. ipyrad: Interactive assembly and analysis of RADseq datasets. Bioinformatics 36(8):2592–2594.

[19]

FormanJ,KesseliRV. 2003. Sexual reproduction in the invasive species Fallopia japonica (Polygonaceae). American Journal of Botany 90(4):586–592.

[20]

FrichotE,François O. 2015. LEA: An R package for landscape and ecological association studies,Methods in Ecology and Evolution 6:925–929.

[21]

GBIF: The Global Biodiversity Information Facility. 2022. GBIF occurrence download. https://doi.org/10.15468/dl.wr2yqp

[22]

GrimsbyJL,Tsirelson D,GammonMA,KesseliR. 2007. Genetic diversity and clonal vs. sexual reproduction in Fallopia spp. (Polygonaceae). American Journal of Botany 94(6):957–964.

[23]

GroeneveldE,BelzileF, LavoieC. 2014. Sexual reproduction of Japanese knotweed (Fallopia japonica s.l.) at its northern distribution limit: New evidence of the effect of climate warming on an invasive species. American Journal of Botany 101(3):459–466.

[24]

HockingS,ToopT, JonesD,Graham I,EastwoodD. 2023. Assessing the relative impacts and economic costs of Japanese knotweed management methods. Scientific Reports 13(1):3872.

[25]

HollingsworthM. 2000. Evidence for massive clonal growth in the invasive weed Fallopia japonica (Japanese Knotweed). Botanical Journal of the Linnean Society 133(4):463–472.

[26]

JombartT,AhmedI. 2011. adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics 27(21):3070–3071.

[27]

JohnsonLR,BregerB, DrummondF. 2019. Novel plant–insect interactions in an urban environment: Enemies, protectors, and pollinators of invasive knotweeds. Ecosphere 10(11):e02885.

[28]

JonesD,BruceG, FowlerMS,Law-Cooper R,GrahamI,AbelA,Street-Perrott FA,EastwoodD. 2018. Optimising physiochemical control of invasive Japanese knotweed. Biological Invasions 20(8):2091–2105.

[29]

KamvarZN,TabimaJF, GrünwaldNJ. 2014. poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281.

[30]

Kato-NoguchiH. 2022. Allelopathy of knotweeds as invasive plants. Plants 11(1):3.

[31]

KimJY,ParkCW. 2000. Morphological and chromosomal variation in Fallopia section Reynoutria (Polygonaceae) in Korea. Brittonia 52(1):34–48.

[32]

S,JosseJ, HussonF. 2008. FactoMineR: An R package for multivariate analysis. Journal of Statistical Software 25(1):1–18.

[33]

LepaisO,WeirJT. 2014. SimRAD: An R package for simulation-based prediction of the number of loci expected in RADseq and similar genotyping by sequencing approaches. Molecular Ecology Resources 14(6):1314–1321.

[34]

MandákB,Bímová K,PyšekP,ŠtěpánekJ,PlačkováI. 2005. Isoenzyme diversity in Reynoutria (Polygonaceae) taxa: Escape from sterility by hybridization. Plant Systematics and Evolution 253(1-4):219–230.

[35]

MandákB,Pyšek P,LysákM,SudaJ,Krahulcová A,BímováK. 2003. Variation in DNA-ploidy levels of Reynoutria taxa in the Czech Republic. Annals of Botany 92(2):265–272.

[36]

Mereďa, Jr.,P,Koláriková Z,HodálováI. 2019. Cytological and morphological variation of Fallopia sect. Reynoutria taxa (Polygonaceae) in the Krivánska Malá Fatra Mountains (Slovakia). Biologia 74(3):215–236.

[37]

Mereďa, Jr.,P,Mártonfiová L,SkokanováK,ŠpanielS,Hodálová I. 2023. Cytogeography of invasive knotweeds (Fallopia sect. Reynoutria) in central Europe: Rare aneuploids and evidence for a climatically determined distribution. Preslia 95(2):241–266.

[38]

PashleyCH. 2003. The use of molecular markers in the study of the origin and evolution of Japanese Knotweed sensu lato. Thesis. Leicester, UK: University of Leicester.

[39]

PetersonBK,WeberJN, KayEH,Fisher HS,HoekstraHE. 2012. Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7(5):e37135.

[40]

PinzoneP,PottsD, PettiboneG,Warren R. 2018. Do novel weapons that degrade mycorrhizal mutualisms promote species invasion? Plant Ecology 219(5):539–548.

[41]

PyšekP,BrockJH, BímováK,MandákB,Jarošík V,Koukolíková I,PerglJ,ŠtěpánekJ. 2003. Vegetative regeneration in invasive Reynoutria (Polygonaceae) taxa: The determinant of invasibility at the genotype level. American Journal of Botany 90(10):1487–1495.

[42]

R Core Team. 2022. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/[accessed 1 May 2022].

[43]

SaratE,Mazaubert E,DutartreA,PouletN,Soubeyran Y. 2015. Les espèces exotiques envahissantes dans les milieux aquatiques: Connaissances pratiques et expériences de gestion. Volume 2—Expériences de gestion. Vincennes, France: Onema Collection Comprendre pour agir. 240.

[44]

Schnitzler-LenobleA,Bailey JA. 2008. Polymorphisme génétique et plasticité phénotypique: Deux atouts pour la dispersion des renouées asiatiques? Revue d’Écologie (La Terre et La Vie) 63(3):209–217.

[45]

ŠolnK,Žnidaršič N,Dolenc KoceJ. 2022. Root growth inhibition and ultrastructural changes in radish root tips after treatment with aqueous extracts of Fallopia japonica and F. × bohemica rhizomes. Protoplasma 259(2):343–355.

[46]

SudaJ,Trávníček P,MandakB,Berchova-BimovaK. 2010. Genome size as a marker for identifying the invasive alien taxa in Fallopia section. Reynoutria. Preslia 82:97–106.

[47]

TiébréMS,Bizoux JP,HardyOJ,BaileyJP,MahyG,2007a. Hybridization and morphogenetic variation in the invasive alien Fallopia (Polygonaceae) complex in Belgium. American Journal of Botany 94(11):1900–1910.

[48]

TiebreMS,Vanderhoeven S,SaadL,MahyG,2007b. Hybridization and sexual reproduction in the invasive alien Fallopia (Polygonaceae) complex in Belgium. Annals of Botany 99(1):193–203.

[49]

VanWallendaelA,AlvarezM, FranksSJ. 2021. Patterns of population genomic diversity in the invasive Japanese knotweed species complex. American Journal of Botany 108(5):857–868.

[50]

VukovićN. 2019. “Flying under the radar”—How misleading distributional data led to wrong appreciation of knotweeds invasion (Reynoutria spp.) in Croatia. BioInvasions Records 8(1):175–189.

[51]

WestonLA,BarneyJN, DiTommasoA. 2005. A review of the biology and ecology of three invasive perennials in New York State: Japanese knotweed (Polygonum cuspidatum), mugwort (Artemisia vulgaris) and pale swallow-wort (Vincetoxicum rossicum). Plant and Soil 277(1-2):53–69.

[52]

ZikaPF,Jacobson AL. 2003. An overlooked hybrid Japanese knotweed (Polygonum cuspidatum × sachalinense; Polygonaceae) in North America. Rhodora 105(922):143–152.

[53]

ZubekS,KapustaP, StanekM,Woch MW,BłaszkowskiJ, StefanowiczAM. 2022. Reynoutria japonica invasion negatively affects arbuscular mycorrhizal fungi communities regardless of the season and soil conditions. Applied Soil Ecology 169:104152.

RIGHTS & PERMISSIONS

2024 The Authors. Journal of Systematics and Evolution published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.

AI Summary AI Mindmap
PDF

128

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/