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Environmental strigolactone drives early growth responses to neighboring plants and soil volume in pea

斯科普斯 生物 生态学 植物 梅德林 生物化学
作者
Cara D. Wheeldon,Maxime Hamon‐Josse,Hannah Lotte Lund,Kaori Yoneyama,Tom Bennett
出处
期刊:Current Biology [Elsevier]
卷期号:32 (16): 3593-3600.e3 被引量:20
标识
DOI:10.1016/j.cub.2022.06.063
摘要

There has been a dramatic recent increase in the understanding of the mechanisms by which plants detect their neighbors,1Bilas R.D. Bretman A. Bennett T. Friends, neighbours and enemies: an overview of the communal and social biology of plants.Plant Cell Environ. 2020; 44: 997-1013https://doi.org/10.1111/pce.13965Crossref PubMed Scopus (35) Google Scholar including by touch,2Markovic D. Nikolic N. Glinwood R. Seisenbaeva G. Ninkovic V. Plant responses to brief touching: a mechanism for early neighbour detection?.PLoS One. 2016; 11: e0165742https://doi.org/10.1371/journal.pone.0165742Crossref PubMed Scopus (21) Google Scholar reflected light,3Roig-Villanova I. Martínez-García J.F. Plant responses to vegetation proximity: a whole life avoiding shade.Front. Plant Sci. 2016; 7: 236https://doi.org/10.3389/fpls.2016.00236Crossref PubMed Scopus (79) Google Scholar volatile organic chemicals, and root exudates.4Ninkovic V. Rensing M. Dahlin I. Markovic D. Who is my neighbor? Volatile cues in plant interactions.Plant Signal. Behav. 2019; 14: 1634993https://doi.org/10.1080/15592324.2019.1634993Crossref PubMed Scopus (65) Google Scholar,5Wang N.Q. Kong C.H. Wang P. Meiners S.J. Root exudate signals in plant-plant interactions.Plant Cell Environ. 2020; 44: 1044-1058https://doi.org/10.1111/pce.13892Crossref PubMed Scopus (72) Google Scholar The importance of root exudates remains ill-defined because of confounding experimental variables6Hess L. De Kroon H. Effects of rooting volume and nutrient availability as an alternative explanation for root self/non-self discrimination.J. Ecol. 2007; 95: 241-251https://doi.org/10.1111/j.1365-2745.2006.01204.xCrossref Scopus (133) Google Scholar,7Semchenko M. Hutchings M.J. John E.A. Challenging the tragedy of the commons in root competition: confounding effects of neighbour presence and substrate volume.J. Ecol. 2007; 95: 252-260https://doi.org/10.1111/j.1365-2745.2007.01210.xCrossref Scopus (99) Google Scholar and difficulties disentangling neighbor detection in shoot and roots.8Elhakeem A. Markovic D. Broberg A. Anten N.P.R. Ninkovic V. Aboveground mechanical stimuli affect belowground plant-plant communication.PLoS One. 2018; 13: e0195646https://doi.org/10.1371/journal.pone.0195646Crossref PubMed Scopus (33) Google Scholar, 9Markovic D. Colzi I. Taiti C. Ray S. Scalone R. Gregory Ali J. Mancuso S. Ninkovic V. Airborne signals synchronize the defenses of neighboring plants in response to touch.J. Exp. Bot. 2019; 70: 691-700https://doi.org/10.1093/jxb/ery375Crossref PubMed Scopus (38) Google Scholar, 10de Wit M. Kegge W. Evers J.B. Vergeer-van Eijk M.H. Gankema P. Voesenek L.A.C.J. Pierik R. Plant neighbor detection through touching leaf tips precedes phytochrome signals.Proc. Natl. Acad. Sci. USA. 2012; 109: 14705-14710https://doi.org/10.1073/pnas.1205437109Crossref PubMed Scopus (74) Google Scholar There is evidence that root exudates allow distinction between kin and non-kin neighbors,11Biedrzycki M.L. Jilany T.A. Dudley S.A. Bais H.P. Root exudates mediate kin recognition in plants.Commun. Integr. Biol. 2010; 3: 28-35https://doi.org/10.4161/cib.3.1.10118Crossref PubMed Scopus (68) Google Scholar, 12Semchenko M. Saar S. Lepik A. Plant root exudates mediate neighbour recognition and trigger complex behavioural changes.New Phytol. 2014; 204: 631-637https://doi.org/10.1111/nph.12930Crossref PubMed Scopus (182) Google Scholar, 13Chen B.J.W. During H.J. Anten N.P.R. Detect thy neighbor: identity recognition at the root level in plants.Plant Sci. 2012; 195: 157-167https://doi.org/10.1016/j.plantsci.2012.07.006Crossref PubMed Scopus (119) Google Scholar but identification of specific exudates that function in neighbor detection and/or kin recognition remain elusive.1Bilas R.D. Bretman A. Bennett T. Friends, neighbours and enemies: an overview of the communal and social biology of plants.Plant Cell Environ. 2020; 44: 997-1013https://doi.org/10.1111/pce.13965Crossref PubMed Scopus (35) Google Scholar Strigolactones (SLs), which are exuded into the soil in significant quantities in flowering plants to promote recruitment of arbuscular mycorrhizal fungi (AMF),14Akiyama K. Matsuzaki K.I. Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi.Nature. 2005; 435: 824-827https://doi.org/10.1038/nature03608Crossref PubMed Scopus (1675) Google Scholar seem intuitive candidates to act as plant-plant signals, since they also act as hormones in plants,15Umehara M. Hanada A. Yoshida S. Akiyama K. Arite T. Takeda-Kamiya N. Magome H. Kamiya Y. Shirasu K. Yoneyama K. et al.Inhibition of shoot branching by new terpenoid plant hormones.Nature. 2008; 455: 195-200https://doi.org/10.1038/nature07272Crossref PubMed Scopus (1489) Google Scholar, 16Gomez-Roldan V. Fermas S. Brewer P.B. Puech-Pagès V. Dun E.A. Pillot J.P. Letisse F. Matusova R. Danoun S. Portais J.C. et al.Strigolactone inhibition of shoot branching.Nature. 2008; 455: 189-194https://doi.org/10.1038/nature07271Crossref PubMed Scopus (1605) Google Scholar, 17Xie X. Yoneyama K. Kisugi T. Nomura T. Akiyama K. Asami T. Yoneyama K. Strigolactones are transported from roots to shoots, although not through the xylem.J. Pesticide Sci. 2015; 40: 214-216https://doi.org/10.1584/jpestics.d15-045Crossref Scopus (0) Google Scholar with dramatic effects on shoot growth18Bennett T. Liang Y. Seale M. Ward S. Müller D. Leyser O. Strigolactone regulates shoot development through a core signalling pathway.Biol. Open. 2016; 5: 1806-1820https://doi.org/10.1242/bio.021402Crossref PubMed Scopus (104) Google Scholar,19Sorefan K. Booker J. Haurogné K. Goussot M. Bainbridge K. Foo E. Chatfield S. Ward S. Beveridge C. Rameau C. Leyser O. MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea.Genes Dev. 2003; 17: 1469-1474https://doi.org/10.1101/gad.256603Crossref PubMed Scopus (485) Google Scholar and milder effects on root development.20Villaécija-Aguilar J.A. Hamon-Josse M. Carbonnel S. Kretschmar A. Schmidt C. Dawid C. Bennett T. Gutjahr C. SMAX1/SMXL2 regulate root and root hair development downstream of KAI2-mediated signalling in Arabidopsis.PLoS Genet. 2019; 15: e1008327https://doi.org/10.1371/journal.pgen.1008327Crossref PubMed Scopus (92) Google Scholar Here, using pea, we test whether SLs act as either cues or signals for neighbor detection. We show that peas detect neighbors early in the life cycle through their root systems, resulting in strong changes in shoot biomass and branching, and that this requires SL biosynthesis. We demonstrate that uptake and detection of SLs exuded by neighboring plants are needed for this early neighbor detection, and that plants that cannot exude SLs are outcompeted by neighboring plants and fail to adjust growth to their soil volume. We conclude that plants both exude SLs as signals to modulate neighbor growth and detect environmental SLs as a cue for neighbor presence; collectively, this allows plants to proactively adjust their shoot growth according to neighbor density.
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