Control of cell proliferation, endoreduplication, cell size, and cell death by the retinoblastoma-related pathway in maize endosperm

Handle URI:
http://hdl.handle.net/10754/562723
Title:
Control of cell proliferation, endoreduplication, cell size, and cell death by the retinoblastoma-related pathway in maize endosperm
Authors:
Sabelli, Paolo A.; Liu, Yan; Dante, Ricardo Augusto; Lizarraga, Lucina E.; Nguyen, Hong N.; Brown, Sara W.; Klingler, John ( 0000-0003-3951-9734 ) ; Yu, Jingjuan; LaBrant, Evan; Layton, Tracy M.; Feldman, Max; Larkins, Brian A.
Abstract:
The endospermof cereal grains is one of the most valuable products of modern agriculture. Cereal endosperm development comprises different phases characterized by mitotic cell proliferation, endoreduplication, the accumulation of storage compounds, and programmed cell death. Although manipulation of these processes could maximize grain yield, how they are regulated and integrated is poorly understood. We show that the Retinoblastoma-related (RBR) pathway controls key aspects of endosperm development in maize. Down-regulation of RBR1 by RNAi resulted in up-regulation of RBR3-type genes, as well as the MINICHROMOSOME MAINTENANCE 2-7 gene family and PROLIFERATING CELL NUCLEAR ANTIGEN, which encode essential DNA replication factors. Both the mitotic and endoreduplication cell cycles were stimulated. Developing transgenic endosperm contained 42-58% more cells and ~70% more DNA than wild type, whereas there was a reduction in cell and nuclear sizes. In addition, cell death was enhanced. The DNA content of mature endosperm increased 43% upon RBR1 downregulation, whereas storage protein content and kernel weight were essentially not affected. Down-regulation of both RBR1 and CYCLIN DEPENDENT KINASE A (CDKA);1 indicated that CDKA;1 is epistatic to RBR1 and controls endoreduplication through an RBR1- dependent pathway. However, the repressive activity of RBR1 on downstream targets was independent from CDKA;1, suggesting diversification of RBR1 activities. Furthermore, RBR1 negatively regulated CDK activity, suggesting the presence of a feedback loop. These results indicate that the RBR1 pathway plays a major role in regulation of different processes during maize endosperm development and suggest the presence of tissue/organlevel regulation of endosperm/seed homeostasis.
KAUST Department:
Center for Desert Agriculture
Publisher:
National Academy of Sciences
Journal:
Proceedings of the National Academy of Sciences of the United States of America
Issue Date:
22-Apr-2013
DOI:
10.1073/pnas.1304903110
PubMed ID:
23610440
PubMed Central ID:
PMC3651506
Type:
Article
ISSN:
00278424
Additional Links:
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3651506
Appears in Collections:
Articles; Center for Desert Agriculture

Full metadata record

DC FieldValue Language
dc.contributor.authorSabelli, Paolo A.en
dc.contributor.authorLiu, Yanen
dc.contributor.authorDante, Ricardo Augustoen
dc.contributor.authorLizarraga, Lucina E.en
dc.contributor.authorNguyen, Hong N.en
dc.contributor.authorBrown, Sara W.en
dc.contributor.authorKlingler, Johnen
dc.contributor.authorYu, Jingjuanen
dc.contributor.authorLaBrant, Evanen
dc.contributor.authorLayton, Tracy M.en
dc.contributor.authorFeldman, Maxen
dc.contributor.authorLarkins, Brian A.en
dc.date.accessioned2015-08-03T11:03:15Zen
dc.date.available2015-08-03T11:03:15Zen
dc.date.issued2013-04-22en
dc.identifier.issn00278424en
dc.identifier.pmid23610440en
dc.identifier.doi10.1073/pnas.1304903110en
dc.identifier.urihttp://hdl.handle.net/10754/562723en
dc.description.abstractThe endospermof cereal grains is one of the most valuable products of modern agriculture. Cereal endosperm development comprises different phases characterized by mitotic cell proliferation, endoreduplication, the accumulation of storage compounds, and programmed cell death. Although manipulation of these processes could maximize grain yield, how they are regulated and integrated is poorly understood. We show that the Retinoblastoma-related (RBR) pathway controls key aspects of endosperm development in maize. Down-regulation of RBR1 by RNAi resulted in up-regulation of RBR3-type genes, as well as the MINICHROMOSOME MAINTENANCE 2-7 gene family and PROLIFERATING CELL NUCLEAR ANTIGEN, which encode essential DNA replication factors. Both the mitotic and endoreduplication cell cycles were stimulated. Developing transgenic endosperm contained 42-58% more cells and ~70% more DNA than wild type, whereas there was a reduction in cell and nuclear sizes. In addition, cell death was enhanced. The DNA content of mature endosperm increased 43% upon RBR1 downregulation, whereas storage protein content and kernel weight were essentially not affected. Down-regulation of both RBR1 and CYCLIN DEPENDENT KINASE A (CDKA);1 indicated that CDKA;1 is epistatic to RBR1 and controls endoreduplication through an RBR1- dependent pathway. However, the repressive activity of RBR1 on downstream targets was independent from CDKA;1, suggesting diversification of RBR1 activities. Furthermore, RBR1 negatively regulated CDK activity, suggesting the presence of a feedback loop. These results indicate that the RBR1 pathway plays a major role in regulation of different processes during maize endosperm development and suggest the presence of tissue/organlevel regulation of endosperm/seed homeostasis.en
dc.publisherNational Academy of Sciencesen
dc.relation.urlhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC3651506en
dc.subjectEndocycleen
dc.subjectSeed developmenten
dc.titleControl of cell proliferation, endoreduplication, cell size, and cell death by the retinoblastoma-related pathway in maize endospermen
dc.typeArticleen
dc.contributor.departmentCenter for Desert Agricultureen
dc.identifier.journalProceedings of the National Academy of Sciences of the United States of Americaen
dc.identifier.pmcidPMC3651506en
dc.contributor.institutionSchool of Plant Sciences, University of Arizona, Tucson, AZ 85721, United Statesen
dc.contributor.institutionState Key Laboratory for Agrobiotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, Chinaen
dc.contributor.institutionHerman B. Wells Center for Pediatric Research, Indiana University School of Medicine, Indianapolis, IN 46202, United Statesen
dc.contributor.institutionEmbrapa Agricultural Informatics, Campinas, SP 13083-886, Brazilen
dc.contributor.institutionPharmacology and Toxicology Department, College of Pharmacy, University of Arizona, Tucson, AZ 85721, United Statesen
dc.contributor.institutionDonald Danforth Plant Science Center, St. Louis, MO 63132, United Statesen
kaust.authorKlingler, Johnen

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