Leaflet initiation and blade expansion are separable in compound leaf development

Fei Du; Yajin Mo; Alon Israeli; Qingqing Wang; Tamar Yifhar; Naomi Ori; Yuling Jiao

doi:10.1111/tpj.14982

Leaflet initiation and blade expansion are separable in compound leaf development

Fei Du^*, Yajin Mo, Alon Israeli, Qingqing Wang, Tamar Yifhar, Naomi Ori, Yuling Jiao

^*Corresponding author for this work

Institute of Plant Sciences and Genetics in Agriculture

Research output: Contribution to journal › Article › peer-review

17 Scopus citations

Abstract

Compound leaves are composed of multiple separate blade units termed leaflets. In tomato (Solanum lycopersicum) compound leaves, auxin promotes both leaflet initiation and blade expansion. However, it is unclear how these two developmental processes interact. With highly variable complexity, tomato compound leaves provide an ideal system to address this question. In this study, we obtained and analyzed mutants of the WUSCHEL-RELATED HOMEOBOX (WOX) family gene SlLAM1 from tomato, whose orthologs in tobacco (Nicotiana sylvestris) and other species are indispensable for blade expansion. We show that SlLAM1 is expressed in the middle and marginal domains of leaves, and is required for blade expansion in leaflets. We demonstrate that sllam1 mutants cause a delay of leaflet initiation and slightly alter the arrangement of first-order leaflets, whereas the overall leaflet number is comparable to that of wild-type leaves. Analysis of the genetic interactions between SlLAM1 and key auxin signaling components revealed an epistatic effect of SlLAM1 in determining the final leaf form. Finally, we show that SlLAM1 is also required for floral organ growth and affects the fertility of gametophytes. Our data suggest that SlLAM1 promotes blade expansion in multiple leaf types, and leaflet initiation can be largely uncoupled from blade expansion during compound leaf morphogenesis.

Original language	American English
Pages (from-to)	1073-1087
Number of pages	15
Journal	Plant Journal
Volume	104
Issue number	4
DOIs	https://doi.org/10.1111/tpj.14982
State	Published - Nov 2020

Bibliographical note

Funding Information:
We thank Prof. Chuanyou Li and Dr. Lei Deng for providing vectors of the tomato CRISPR/Cas9 system, Prof. Gang Wu and Dr. Yunmin Xu for seeds, and Prof. Yuval Eshed for information, materials, and insights. This work was supported by NSFC grants 31861143021 and 31825002, the Key Research Project of the Frontier Science of the Chinese Academy of Sciences grant ZDBS‐LY‐SM012, and ISF grants 248/19 and ISF‐NSFC 2407/18. Alon Israeli is grateful to the Azrieli Foundation for the award of an Azrieli Fellowship. kan1‐12 kan2

Publisher Copyright:
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd

Keywords

SlLAM1
SlWOX1
Solanum lycopersicum
auxin
blastozone
compound leaf
flower development
leaf meristem
tomato

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10.1111/tpj.14982

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@article{2a8e785e34c84e1b93e82d5f60c1630a,

title = "Leaflet initiation and blade expansion are separable in compound leaf development",

abstract = "Compound leaves are composed of multiple separate blade units termed leaflets. In tomato (Solanum lycopersicum) compound leaves, auxin promotes both leaflet initiation and blade expansion. However, it is unclear how these two developmental processes interact. With highly variable complexity, tomato compound leaves provide an ideal system to address this question. In this study, we obtained and analyzed mutants of the WUSCHEL-RELATED HOMEOBOX (WOX) family gene SlLAM1 from tomato, whose orthologs in tobacco (Nicotiana sylvestris) and other species are indispensable for blade expansion. We show that SlLAM1 is expressed in the middle and marginal domains of leaves, and is required for blade expansion in leaflets. We demonstrate that sllam1 mutants cause a delay of leaflet initiation and slightly alter the arrangement of first-order leaflets, whereas the overall leaflet number is comparable to that of wild-type leaves. Analysis of the genetic interactions between SlLAM1 and key auxin signaling components revealed an epistatic effect of SlLAM1 in determining the final leaf form. Finally, we show that SlLAM1 is also required for floral organ growth and affects the fertility of gametophytes. Our data suggest that SlLAM1 promotes blade expansion in multiple leaf types, and leaflet initiation can be largely uncoupled from blade expansion during compound leaf morphogenesis.",

keywords = "SlLAM1, SlWOX1, Solanum lycopersicum, auxin, blastozone, compound leaf, flower development, leaf meristem, tomato",

author = "Fei Du and Yajin Mo and Alon Israeli and Qingqing Wang and Tamar Yifhar and Naomi Ori and Yuling Jiao",

note = "Funding Information: We thank Prof. Chuanyou Li and Dr. Lei Deng for providing vectors of the tomato CRISPR/Cas9 system, Prof. Gang Wu and Dr. Yunmin Xu for seeds, and Prof. Yuval Eshed for information, materials, and insights. This work was supported by NSFC grants 31861143021 and 31825002, the Key Research Project of the Frontier Science of the Chinese Academy of Sciences grant ZDBS‐LY‐SM012, and ISF grants 248/19 and ISF‐NSFC 2407/18. Alon Israeli is grateful to the Azrieli Foundation for the award of an Azrieli Fellowship. kan1‐12 kan2 Publisher Copyright: {\textcopyright} 2020 Society for Experimental Biology and John Wiley & Sons Ltd",

year = "2020",

month = nov,

doi = "10.1111/tpj.14982",

language = "American English",

volume = "104",

pages = "1073--1087",

journal = "Plant Journal",

issn = "0960-7412",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "4",

}

TY - JOUR

T1 - Leaflet initiation and blade expansion are separable in compound leaf development

AU - Du, Fei

AU - Mo, Yajin

AU - Israeli, Alon

AU - Wang, Qingqing

AU - Yifhar, Tamar

AU - Ori, Naomi

AU - Jiao, Yuling

N1 - Funding Information: We thank Prof. Chuanyou Li and Dr. Lei Deng for providing vectors of the tomato CRISPR/Cas9 system, Prof. Gang Wu and Dr. Yunmin Xu for seeds, and Prof. Yuval Eshed for information, materials, and insights. This work was supported by NSFC grants 31861143021 and 31825002, the Key Research Project of the Frontier Science of the Chinese Academy of Sciences grant ZDBS‐LY‐SM012, and ISF grants 248/19 and ISF‐NSFC 2407/18. Alon Israeli is grateful to the Azrieli Foundation for the award of an Azrieli Fellowship. kan1‐12 kan2 Publisher Copyright: © 2020 Society for Experimental Biology and John Wiley & Sons Ltd

PY - 2020/11

Y1 - 2020/11

N2 - Compound leaves are composed of multiple separate blade units termed leaflets. In tomato (Solanum lycopersicum) compound leaves, auxin promotes both leaflet initiation and blade expansion. However, it is unclear how these two developmental processes interact. With highly variable complexity, tomato compound leaves provide an ideal system to address this question. In this study, we obtained and analyzed mutants of the WUSCHEL-RELATED HOMEOBOX (WOX) family gene SlLAM1 from tomato, whose orthologs in tobacco (Nicotiana sylvestris) and other species are indispensable for blade expansion. We show that SlLAM1 is expressed in the middle and marginal domains of leaves, and is required for blade expansion in leaflets. We demonstrate that sllam1 mutants cause a delay of leaflet initiation and slightly alter the arrangement of first-order leaflets, whereas the overall leaflet number is comparable to that of wild-type leaves. Analysis of the genetic interactions between SlLAM1 and key auxin signaling components revealed an epistatic effect of SlLAM1 in determining the final leaf form. Finally, we show that SlLAM1 is also required for floral organ growth and affects the fertility of gametophytes. Our data suggest that SlLAM1 promotes blade expansion in multiple leaf types, and leaflet initiation can be largely uncoupled from blade expansion during compound leaf morphogenesis.

AB - Compound leaves are composed of multiple separate blade units termed leaflets. In tomato (Solanum lycopersicum) compound leaves, auxin promotes both leaflet initiation and blade expansion. However, it is unclear how these two developmental processes interact. With highly variable complexity, tomato compound leaves provide an ideal system to address this question. In this study, we obtained and analyzed mutants of the WUSCHEL-RELATED HOMEOBOX (WOX) family gene SlLAM1 from tomato, whose orthologs in tobacco (Nicotiana sylvestris) and other species are indispensable for blade expansion. We show that SlLAM1 is expressed in the middle and marginal domains of leaves, and is required for blade expansion in leaflets. We demonstrate that sllam1 mutants cause a delay of leaflet initiation and slightly alter the arrangement of first-order leaflets, whereas the overall leaflet number is comparable to that of wild-type leaves. Analysis of the genetic interactions between SlLAM1 and key auxin signaling components revealed an epistatic effect of SlLAM1 in determining the final leaf form. Finally, we show that SlLAM1 is also required for floral organ growth and affects the fertility of gametophytes. Our data suggest that SlLAM1 promotes blade expansion in multiple leaf types, and leaflet initiation can be largely uncoupled from blade expansion during compound leaf morphogenesis.

KW - SlLAM1

KW - SlWOX1

KW - Solanum lycopersicum

KW - auxin

KW - blastozone

KW - compound leaf

KW - flower development

KW - leaf meristem

KW - tomato

UR - http://www.scopus.com/inward/record.url?scp=85091438400&partnerID=8YFLogxK

U2 - 10.1111/tpj.14982

DO - 10.1111/tpj.14982

M3 - Article

C2 - 32889762

AN - SCOPUS:85091438400

SN - 0960-7412

VL - 104

SP - 1073

EP - 1087

JO - Plant Journal

JF - Plant Journal

IS - 4

ER -

Leaflet initiation and blade expansion are separable in compound leaf development

Abstract

Bibliographical note

Keywords

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