The bHLH transcription factor SPATULA enables cytokinin signaling, and both activate auxin biosynthesis and transport genes at the medial domain of the gynoecium

• Published in: PLoS genetics Vol. 13; no. 4; p. e1006726
• Main Authors: Reyes-Olalde, J Irepan, Zúñiga-Mayo, Víctor M, Serwatowska, Joanna, Chavez Montes, Ricardo A, Lozano-Sotomayor, Paulina, Herrera-Ubaldo, Humberto, Gonzalez-Aguilera, Karla L, Ballester, Patricia, Ripoll, Juan José, Ezquer, Ignacio, Paolo, Dario, Heyl, Alexander, Colombo, Lucia, Yanofsky, Martin F, Ferrandiz, Cristina, Marsch-Martínez, Nayelli, de Folter, Stefan
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 07-04-2017; Public Library of Science (PLoS)
• Subjects: Angiosperms; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Assaying; Basic Helix-Loop-Helix Transcription Factors - genetics; Basic Helix-Loop-Helix Transcription Factors - metabolism; Binding sites; Biology and Life Sciences; Biosynthesis; Carpels; Colleges & universities; Confocal microscopy; Coordinate measuring machines; Cytokinins; Cytokinins - metabolism; Drainage; Fertilization; Fertilizing; Flowering; Flowers - genetics; Flowers - growth & development; Food sources; Fruit - genetics; Fruit - growth & development; Fruits; Gene expression; Gene Expression Regulation, Plant; Genes; Genetic aspects; Genomics; Germination; Helix-loop-helix proteins (basic); Histidine; Huntingtin; Huntington's disease; Indoleacetic Acids - metabolism; Integration; Medicine and Health Sciences; Meristem - genetics; Meristem - growth & development; Neurodegenerative diseases; Nuclei; Nuclei (cytology); Ovules; Phosphotransferase; Physiological aspects; Plant cells; Polymerase chain reaction; Protein interaction; Proteins; Repressors; Research and Analysis Methods; Ribonuclease; Screens; Seeds; Seeds - genetics; Seeds - growth & development; Septum; Signal Transduction; Transcription factors; Tryptophan Transaminase - genetics; United States > US; California
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1006726

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.