TY - JOUR
T1 - The Sequential Action of MIDA9/PP2C.D1, PP2C.D2, and PP2C.D5 Is Necessary to Form and Maintain the Hook After Germination in the Dark
AU - Rovira, Arnau
AU - Sentandreu, Maria
AU - Nagatani, Akira
AU - Leivar, Pablo
AU - Monte, Elena
N1 - Funding Information:
This work was supported by a “Comissionat per a Universitats i Recerca del Departament d’Innovació, Universitats i Empresa” fellowship of the Generalitat de Catalunya (Beatriu de Pino’s program) and Marie Curie IRG PIRG06-GA-2009-256420 grant to PL, by grants from FEDER/Ministerio de Ciencia, Innovación y Universidades – Agencia Estatal de Investigación (project references BIO2009-07675, BIO2015-68460-P, and
Funding Information:
We thank Martí Bernardo-Faura (Molecular Data Analysis Area, CRAG) for his support with the statistical analysis in Figure 5C. Funding. This work was supported by a “Comissionat per a Universitats i Recerca del Departament d’Innovació, Universitats i Empresa” fellowship of the Generalitat de Catalunya (Beatriu de Pino’s program) and Marie Curie IRG PIRG06-GA-2009-256420 grant to PL, by grants from FEDER/Ministerio de Ciencia, Innovación y Universidades – Agencia Estatal de Investigación (project references BIO2009-07675, BIO2015-68460-P, and PGC2018-099987-B-I00) and from the CERCA Programme/Generalitat de Catalunya (project references 2009-SGR-206 and 2017SGR-718) to EM. MS was recipient of a travel fellowship from the “Comissionat per a Universitats i Recerca del Departament d’Innovacio, Universitats i Empresa” of the Generalitat de Catalunya. We acknowledge financial support from the Spanish Ministry of Economy and Competitiveness, through the “Severo Ochoa Programme for Centres of Excellence in R&D” 2016–2019 (SEV-2015-0533) and support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).
Publisher Copyright:
© Copyright © 2021 Rovira, Sentandreu, Nagatani, Leivar and Monte.
PY - 2021/3/9
Y1 - 2021/3/9
N2 - During seedling etiolation after germination in the dark, seedlings have closed cotyledons and form an apical hook to protect the meristem as they break through the soil to reach the surface. Once in contact with light, the hook opens and cotyledons are oriented upward and separate. Hook development in the dark after seedling emergence from the seed follows three distinctly timed and sequential phases: formation, maintenance, and eventual opening. We previously identified MISREGULATED IN DARK9 (MIDA9) as a phytochrome interacting factor (PIF)-repressed gene in the dark necessary for hook development during etiolated growth. MIDA9 encodes the type 2C phosphatase PP2C.D1, and pp2c-d1/mida9 mutants exhibit open hooks in the dark. Recent evidence has described that PP2C.D1 and other PP2C.D members negatively regulate SMALL AUXIN UP RNA (SAUR)-mediated cell elongation. However, the fundamental question of the timing of PP2C.D1 action (and possibly other members of the PP2C.D family) during hook development remains to be addressed. Here, we show that PP2C.D1 is required immediately after germination to form the hook. pp2c.d1/mida9 shows reduced cell expansion in the outer layer of the hook and, therefore, does not establish the differential cell growth necessary for hook formation, indicating that PP2C.D1 is necessary to promote cell elongation during this early stage. Additionally, genetic analyses of single and high order mutants in PP2C.D1, PP2C.D2, and PP2C.D5 demonstrate that the three PP2C.Ds act collectively and sequentially during etiolation: whereas PP2C.D1 dominates hook formation, PP2C.D2 is necessary during the maintenance phase, and PP2C.D5 acts to prevent opening during the third phase together with PP2C.D1 and PP2C.D2. Finally, we uncover a possible connection of PP2C.D1 levels with ethylene physiology, which could help optimize hook formation during post-germinative growth in the dark.
AB - During seedling etiolation after germination in the dark, seedlings have closed cotyledons and form an apical hook to protect the meristem as they break through the soil to reach the surface. Once in contact with light, the hook opens and cotyledons are oriented upward and separate. Hook development in the dark after seedling emergence from the seed follows three distinctly timed and sequential phases: formation, maintenance, and eventual opening. We previously identified MISREGULATED IN DARK9 (MIDA9) as a phytochrome interacting factor (PIF)-repressed gene in the dark necessary for hook development during etiolated growth. MIDA9 encodes the type 2C phosphatase PP2C.D1, and pp2c-d1/mida9 mutants exhibit open hooks in the dark. Recent evidence has described that PP2C.D1 and other PP2C.D members negatively regulate SMALL AUXIN UP RNA (SAUR)-mediated cell elongation. However, the fundamental question of the timing of PP2C.D1 action (and possibly other members of the PP2C.D family) during hook development remains to be addressed. Here, we show that PP2C.D1 is required immediately after germination to form the hook. pp2c.d1/mida9 shows reduced cell expansion in the outer layer of the hook and, therefore, does not establish the differential cell growth necessary for hook formation, indicating that PP2C.D1 is necessary to promote cell elongation during this early stage. Additionally, genetic analyses of single and high order mutants in PP2C.D1, PP2C.D2, and PP2C.D5 demonstrate that the three PP2C.Ds act collectively and sequentially during etiolation: whereas PP2C.D1 dominates hook formation, PP2C.D2 is necessary during the maintenance phase, and PP2C.D5 acts to prevent opening during the third phase together with PP2C.D1 and PP2C.D2. Finally, we uncover a possible connection of PP2C.D1 levels with ethylene physiology, which could help optimize hook formation during post-germinative growth in the dark.
KW - MIDA9
KW - PP2C.D phosphatases
KW - ethylene
KW - etiolation
KW - hook
KW - phytochrome interacting factor PIF
KW - skotomorphogenesis
UR - http://www.scopus.com/inward/record.url?scp=85103136895&partnerID=8YFLogxK
U2 - 10.3389/fpls.2021.636098
DO - 10.3389/fpls.2021.636098
M3 - Article
AN - SCOPUS:85103136895
SN - 1664-462X
VL - 12
JO - Frontiers in Plant Science
JF - Frontiers in Plant Science
M1 - 636098
ER -