ARABIDOPSIS HOMOLOG OF TRITHORAX1 impacts lateral root development by epigenetic regulation of targets involved in root system architecture

被引:0
作者
Napsucialy-Mendivil, Selene [1 ]
Torres-Martinez, Hector H. [1 ,2 ]
Rodriguez-Alonso, Gustavo [3 ]
Rivera-Toro, Diana Marcela [4 ]
Alvarez-Venegas, Raul [4 ]
Juarez-Verdayes, Marco Adan [1 ,5 ]
Shishkova, Svetlana [1 ]
Dubrovsky, Joseph G. [1 ]
机构
[1] Univ Nacl Autonoma Mexico, Dept Biol Mol Plantas, Inst Biotecnol, Cuernavaca 62210, Morelos, Mexico
[2] Stanford Univ, Dept Biol, Stanford, CA 94305 USA
[3] Univ Autonoma Estado Morelos, Ctr Invest Dinam Celular, Inst Invest Ciencias Basicas & Aplicadas, Cuernavaca 62209, Morelos, Mexico
[4] Inst Politecn Nacl, Ctr Invest & Estudios Avanzados, CINVESTAV IPN, Unidad Irapuato, Irapuato 36824, Guanajuato, Mexico
[5] Univ Autonoma Agr Antonio Narro, Dept Ciencias Basicas, Saltillo 25315, Coahuila, Mexico
关键词
cell cycle; epigenetic regulation; lateral roots; live imaging; methyltransferase activity; morphogenesis; reactive oxygen species; transcriptomics; MADS-BOX GENE; CELL-PROLIFERATION; QUIESCENT CENTER; ARABIDOPSIS; PLANT; INITIATION; TRITHORAX; ORGANIZATION; COMPLEX; CYCLE;
D O I
10.1111/nph.70349
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Developmental processes are regulated at multiple levels, including the epigenetic level. Among the epigenetic factors, histone H3 lysine 4 (H3K4) methyltransferases contribute to active transcription of target genes, and here, we explored how the H3K4 methyltransferase ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) affects Arabidopsis thaliana lateral root (LR) primordium (LRP) morphogenesis. We examined LR development in a loss-of-function null mutant (atx1-1) and a mutant affected in the ATX1 catalytic domain (atx1setm) through bright-field and long-term time-lapse confocal microscopy, transcriptomics, and chromatin immunoprecipitation. LRP morphogenesis in both mutants was severely abnormal, resulting from altered principal growth directions, and was accompanied by extended cell cycle durations and slower transitions between LRP stages. Among the differentially expressed genes downregulated in atx1setm, the most enriched Gene Ontology categories were cell wall organization and H2O2 metabolism, the latter of which included PEROXIDASE35 (PRX35). The LRP morphogenesis abnormalities were similar in prx35 and atx1 mutants. Both the deposition of H3K4me3 at the PRX35 promoter and the PRX35 expression in the atx1setm mutant were significantly reduced. Our results reveal a link between LR development and a redox homeostasis controlled by ATX1 at epigenetic level by maintaining active transcription of PRX35 and thereby impacting root system formation. Los procesos de desarrollo est & aacute;n regulados a diferentes niveles incluyendo el nivel epigen & eacute;tico. La histona metiltransferasa (H3K4me) es un factor epigen & eacute;tico que contribuye a la transcripci & oacute;n activa de sus genes diana. En este trabajo exploramos, como la H3K4 metiltransferasa ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) afecta la morfog & eacute;nesis del primordio de ra & iacute;z lateral, proceso fundamental para que la ra & iacute;z lateral se desarrolle adecuadamente. Usando diferentes enfoques, tales como microscop & iacute;a de campo claro y confocal, experimentos de rastreo celular en tejidos vivos, an & aacute;lisis del transcriptoma e inmunoprecipitaci & oacute;n de la cromatina, estudiamos el desarrollo de la ra & iacute;z lateral en una mutante nula de p & eacute;rdida de funci & oacute;n (atx1-1) y en una mutante afectada en el dominio catal & iacute;tico de ATX1 (atx1setm), ambas en planta modelo Arabidopsis thaliana. Encontramos que la morfog & eacute;nesis del primordio de ra & iacute;z lateral result & oacute; severamente afectada en las mutantes como consecuencia del cambio en la direcci & oacute;n principal del crecimiento, del ciclo celular alargado y de las transiciones lentas entre los estadios del desarrollo de los primordios. Las categorias de ontolog & iacute;a de genes m & aacute;s enriquecidas entre los genes diferencialmente expresados que bajaron su abundancia en la mutante atx1-1, fueron la organizaci & oacute;n de la pared celular y el metabolismo del per & oacute;xido de hidrogeno, dentro de esta & uacute;ltima categor & iacute;a se encontr & oacute; a la PEROXIDASE35 (PRX35). Las anomal & iacute;as en la morfog & eacute;nesis de los primordios de ra & iacute;z lateral en las mutantes prx35 fueron similares a las anomal & iacute;as encontradas en atx1. Evidenciamos que en la mutante atx1setm tanto la deposici & oacute;n de la marca H3K4me3 en el promotor de PRX35 como su expresi & oacute;n se disminuyeron significativamente, lo que sugiere que ATX1 regula a PRX35 y ambos genes son esenciales para el desarrollo de la ra & iacute;z en plantas. Este trabajo revelo una asociaci & oacute;n entre el control del desarrollo de la ra & iacute;z lateral a nivel epigen & eacute;tico y la homeostasis del estado redox, involucrado en la morfog & eacute;nesis del primordio de la ra & iacute;z lateral. Esta asociaci & oacute;n impacta el control de la arquitectura del sistema radical en plantas.
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