title: The bHLH transcription factor SPATULA enables cytokinin signaling, and both activate auxin biosynthesis and transport genes at the medial domain of the gynoecium.
abstract: Fruits and seeds are the major food source on earth. Both derive from the gynoecium and, therefore, it is crucial to understand the mechanisms that guide the development of this organ of angiosperm species. In Arabidopsis, the gynoecium is composed of two congenitally fused carpels, where two domains: medial and lateral, can be distinguished. The medial domain includes the carpel margin meristem (CMM) that is key for the production of the internal tissues involved in fertilization, such as septum, ovules, and transmitting tract. Interestingly, the medial domain shows a high cytokinin signaling output, in contrast to the lateral domain, where it is hardly detected. While it is known that cytokinin provides meristematic properties, understanding on the mechanisms that underlie the cytokinin signaling pattern in the young gynoecium is lacking. Moreover, in other tissues, the cytokinin pathway is often connected to the auxin pathway, but we also lack knowledge about these connections in the young gynoecium. Our results reveal that cytokinin signaling, that can provide meristematic properties required for CMM activity and growth, is enabled by the transcription factor SPATULA (SPT) in the medial domain. Meanwhile, cytokinin signaling is confined to the medial domain by the cytokinin response repressor ARABIDOPSIS HISTIDINE PHOSPHOTRANSFERASE 6 (AHP6), and perhaps by ARR16 (a type-A ARR) as well, both present in the lateral domains (presumptive valves) of the developing gynoecia. Moreover, SPT and cytokinin, probably together, promote the expression of the auxin biosynthetic gene TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) and the gene encoding the auxin efflux transporter PIN-FORMED 3 (PIN3), likely creating auxin drainage important for gynoecium growth. This study provides novel insights in the spatiotemporal determination of the cytokinin signaling pattern and its connection to the auxin pathway in the young gynoecium.
authors.affiliation: Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, México.
authors.forename: J Irepan
authors.initials: JI
authors.lastname: Reyes-Olalde
authors.affiliation: Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, México.
authors.forename: Víctor M
authors.initials: VM
authors.lastname: Zúñiga-Mayo
authors.affiliation: Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, México.
authors.forename: Joanna
authors.identifier: 0000-0001-9256-0053
authors.initials: J
authors.lastname: Serwatowska
authors.affiliation: Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, México.
authors.forename: Ricardo A
authors.identifier: 0000-0001-6132-8956
authors.initials: RA
authors.lastname: Chavez Montes
authors.affiliation: Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, México.
authors.forename: Paulina
authors.identifier: 0000-0002-3933-0002
authors.initials: P
authors.lastname: Lozano-Sotomayor
authors.affiliation: Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, México.
authors.forename: Humberto
authors.identifier: 0000-0002-5408-4022
authors.initials: H
authors.lastname: Herrera-Ubaldo
authors.affiliation: Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, México.
authors.forename: Karla L
authors.initials: KL
authors.lastname: Gonzalez-Aguilera
authors.affiliation: Instituto de Biología Molecular y Celular de Plantas, CSIC-UPV Universidad Politécnica de Valencia, Valencia, Spain.
authors.forename: Patricia
authors.initials: P
authors.lastname: Ballester
authors.affiliation: Division of Biological Sciences, University of California San Diego, La Jolla, California, United States of America.
authors.forename: Juan José
authors.identifier: 0000-0002-8229-1555
authors.initials: JJ
authors.lastname: Ripoll
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, Milan, Italy.
authors.forename: Ignacio
authors.identifier: 0000-0003-1886-0095
authors.initials: I
authors.lastname: Ezquer
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, Milan, Italy.
authors.forename: Dario
authors.initials: D
authors.lastname: Paolo
authors.affiliation: Biology Department, Adelphi University, Garden City, New York, United States of America.
authors.forename: Alexander
authors.identifier: 0000-0002-8782-1260
authors.initials: A
authors.lastname: Heyl
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, Milan, Italy.
authors.forename: Lucia
authors.identifier: 0000-0001-8415-1399
authors.initials: L
authors.lastname: Colombo
authors.affiliation: Division of Biological Sciences, University of California San Diego, La Jolla, California, United States of America.
authors.forename: Martin F
authors.initials: MF
authors.lastname: Yanofsky
authors.affiliation: Instituto de Biología Molecular y Celular de Plantas, CSIC-UPV Universidad Politécnica de Valencia, Valencia, Spain.
authors.forename: Cristina
authors.initials: C
authors.lastname: Ferrandiz
authors.affiliation: Departamento de Biotecnología y Bioquímica, CINVESTAV-IPN, Irapuato, Guanajuato, México.
authors.forename: Nayelli
authors.initials: N
authors.lastname: Marsch-Martínez
authors.affiliation: Unidad de Genómica Avanzada (LANGEBIO), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato, México.
authors.forename: Stefan
authors.identifier: 0000-0003-4363-7274
authors.initials: S
authors.lastname: de Folter
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D051792:Basic Helix-Loop-Helix Proteins / Q000235:genetics* / Q000378:metabolism; D003583:Cytokinins / Q000378:metabolism*; D035264:Flowers / Q000235:genetics / Q000254:growth & development; D005638:Fruit / Q000235:genetics / Q000254:growth & development; D018506:Gene Expression Regulation, Plant; D007210:Indoleacetic Acids / Q000378:metabolism; D018519:Meristem / Q000235:genetics* / Q000254:growth & development; D012639:Seeds / Q000235:genetics / Q000254:growth & development; D015398:Signal Transduction; D051279:Tryptophan Transaminase / Q000235:genetics
chemical_list: D029681:Arabidopsis Proteins; D051792:Basic Helix-Loop-Helix Proteins; D003583:Cytokinins; D007210:Indoleacetic Acids; D051279:Tryptophan Transaminase; C507179:AHP6 protein, Arabidopsis; C470378:ARR16 protein, Arabidopsis; C449300:PIN3 protein, Arabidopsis; C426006:SPT protein, Arabidopsis