TY - JOUR
T1 - Developmental genetics of corolla tube formation
T2 - Role of the tasiRNA-ARF pathway and a conceptual model
AU - Ding, Baoqing
AU - Xia, Rui
AU - Lin, Qiaoshan
AU - Gurung, Vandana
AU - Sagawa, Janelle M.
AU - Stanley, Lauren E.
AU - Strobel, Matthew
AU - Diggle, Pamela K.
AU - Meyers, Blake C.
AU - Yuan, Yao Wu
N1 - Funding Information:
We thank Toby Bradshaw (University of Washington) for encouragement and initial support for generating the bulk-segregant data in his laboratory. We thank Clinton Morse, Matt Opel, and Adam Histen for plant care in the University of Connecticut EEB Research Greenhouses. We thank Kun Huang (University of Delaware) for help in examining the spatial pattern of MlARF4 expression. The DR5rev:mRFPer plasmid was kindly provided by David Jackson (Cold Spring Harbor Laboratory). We thank the editors and three anonymous reviewers for their constructive criticism, which greatly improved the article. This work was supported by University of Connecticut start-up funds and the NSF j BIO j Division of Integrative Organismal Systems (grants IOS-1755373 and IOS-1827645 to Y.-W.Y. and grant IOS-1257869 to B.C.M.).
Funding Information:
We thank Toby Bradshaw (University of Washington) for encouragement and initial support for generating the bulk-segregant data in his laboratory. We thank Clinton Morse, Matt Opel, and Adam Histen for plant care in the University of Connecticut EEB Research Greenhouses. We thank Kun Huang (University of Delaware) for help in examining the spatial pattern of MlARF4 expression. The DR5rev:mRFPer plasmid was kindly provided by David Jackson (Cold Spring Harbor Laboratory). We thank the editors and three anonymous reviewers for their constructive criticism, which greatly improved the article. This work was supported by University of Connecticut start-up funds and the NSF | BIO | Division of Integrative Organismal Systems (grants IOS-1755373 and IOS-1827645 to Y.-W.Y. and grant IOS-1257869 to B.C.M.).
Publisher Copyright:
© 2020 ASPB.
PY - 2020/11/1
Y1 - 2020/11/1
N2 - Over 80,000 angiosperm species produce flowers with petals fused into a corolla tube. The corolla tube contributes to the tremendous diversity of flower morphology and plays a critical role in plant reproduction, yet it remains one of the least understood plant structures from a developmental genetics perspective. Through mutant analyses and transgenic experiments, we show that the tasiRNA-ARF pathway is required for corolla tube formation in the monkeyflower species Mimulus lewisii. Loss-of-function mutations in the M. lewisii orthologs of ARGONAUTE7 and SUPPRESSOR OF GENE SILENCING3 cause a dramatic decrease in abundance of TAS3-derived small RNAs and a moderate upregulation of AUXIN RESPONSE FACTOR3 (ARF3) and ARF4, which lead to inhibition of lateral expansion of the bases of petal primordia and complete arrest of the upward growth of the interprimordial regions, resulting in unfused corollas. Using the DR5 auxin-responsive promoter, we discovered that auxin signaling is continuous along the petal primordium base and the interprimordial region during the critical stage of corolla tube formation in the wild type, similar to the spatial pattern of MlARF4 expression. Auxin response is much weaker and more restricted in the mutant. Furthermore, exogenous application of a polar auxin transport inhibitor to wild-type floral apices disrupted petal fusion. Together, these results suggest a new conceptual model highlighting the central role of auxin-directed synchronized growth of the petal primordium base and the interprimordial region in corolla tube formation.
AB - Over 80,000 angiosperm species produce flowers with petals fused into a corolla tube. The corolla tube contributes to the tremendous diversity of flower morphology and plays a critical role in plant reproduction, yet it remains one of the least understood plant structures from a developmental genetics perspective. Through mutant analyses and transgenic experiments, we show that the tasiRNA-ARF pathway is required for corolla tube formation in the monkeyflower species Mimulus lewisii. Loss-of-function mutations in the M. lewisii orthologs of ARGONAUTE7 and SUPPRESSOR OF GENE SILENCING3 cause a dramatic decrease in abundance of TAS3-derived small RNAs and a moderate upregulation of AUXIN RESPONSE FACTOR3 (ARF3) and ARF4, which lead to inhibition of lateral expansion of the bases of petal primordia and complete arrest of the upward growth of the interprimordial regions, resulting in unfused corollas. Using the DR5 auxin-responsive promoter, we discovered that auxin signaling is continuous along the petal primordium base and the interprimordial region during the critical stage of corolla tube formation in the wild type, similar to the spatial pattern of MlARF4 expression. Auxin response is much weaker and more restricted in the mutant. Furthermore, exogenous application of a polar auxin transport inhibitor to wild-type floral apices disrupted petal fusion. Together, these results suggest a new conceptual model highlighting the central role of auxin-directed synchronized growth of the petal primordium base and the interprimordial region in corolla tube formation.
UR - http://www.scopus.com/inward/record.url?scp=85095460901&partnerID=8YFLogxK
U2 - 10.1105/TPC.18.00471
DO - 10.1105/TPC.18.00471
M3 - Article
C2 - 32917737
AN - SCOPUS:85095460901
SN - 1040-4651
VL - 32
SP - 3452
EP - 3468
JO - Plant Cell
JF - Plant Cell
IS - 11
ER -