Dual functions of Macpiwi1 in transposon silencing and stem cell maintenance in the flatworm Macrostomum lignano.
PIWI proteins and piRNA pathways are essential for transposon silencing and some aspects of gene regulation during animal germline development. In contrast to most animal species, some flatworms also express PIWIs and piRNAs in somatic stem cells, where they are required for tissue renewal and regeneration. Here, we have identified and characterized piRNAs and PIWI proteins in the emerging model flatworm Macrostomum lignano. We found that M. lignano encodes at least three PIWI proteins. One of these, Macpiwi1, acts as a key component of the canonical piRNA pathway in the germline and in somatic stem cells. Knockdown of Macpiwi1 dramatically reduces piRNA levels, derepresses transposons, and severely impacts stem cell maintenance. Knockdown of the piRNA biogenesis factor Macvasa caused an even greater reduction in piRNA levels with a corresponding increase in transposons. Yet, in Macvasa knockdown animals, we detected no major impact on stem cell self-renewal. These results may suggest stem cell maintenance functions of PIWI proteins in flatworms that are distinguishable from their impact on transposons and that might function independently of what are considered canonical piRNA populations.
Cold Spring Harbor Laboratory and Watson School of Biological Sciences, Cold Spring Harbor, New York 11724, USA Molecular and Cellular Biology Graduate Program, Stony Brook University, Stony Brook, New York 11794, USA.
Xin
X
Zhou
Cold Spring Harbor Laboratory and Watson School of Biological Sciences, Cold Spring Harbor, New York 11724, USA.
Giorgia
G
Battistoni
Cold Spring Harbor Laboratory and Watson School of Biological Sciences, Cold Spring Harbor, New York 11724, USA.
Osama
O
El Demerdash
Cold Spring Harbor Laboratory and Watson School of Biological Sciences, Cold Spring Harbor, New York 11724, USA.
James
J
Gurtowski
University of Innsbruck, Institute of Zoology and CMBI, A-6020 Innsbruck, Austria.
Julia
J
Wunderer
Cold Spring Harbor Laboratory and Watson School of Biological Sciences, Cold Spring Harbor, New York 11724, USA.
Ilaria
I
Falciatori
University of Innsbruck, Institute of Zoology and CMBI, A-6020 Innsbruck, Austria.
Peter
P
Ladurner
Cold Spring Harbor Laboratory and Watson School of Biological Sciences, Cold Spring Harbor, New York 11724, USA.
Michael C
MC
Schatz
Cold Spring Harbor Laboratory and Watson School of Biological Sciences, Cold Spring Harbor, New York 11724, USA CRUK Cambridge Institute, Li Ka Shing Centre, University of Cambridge, Cambridge CB2 0RE, United Kingdom.
Gregory J
GJ
Hannon
Cold Spring Harbor Laboratory and Watson School of Biological Sciences, Cold Spring Harbor, New York 11724, USA.
Kaja A
KA
Wasik
D000818:Animals; D060565:Argonaute Proteins / Q000378:metabolism*; D004251:DNA Transposable Elements / Q000235:genetics*; D005786:Gene Expression Regulation / Q000235:genetics; D020868:Gene Silencing / Q000502:physiology*; D005854:Germ Cells / Q000378:metabolism; D010986:Platyhelminths / Q000235:genetics* / Q000378:metabolism*; D034741:RNA, Small Interfering / Q000235:genetics; D012038:Regeneration / Q000235:genetics; D013234:Stem Cells / Q000378:metabolism*
D060565:Argonaute Proteins; D004251:DNA Transposable Elements; D034741:RNA, Small Interfering
Macrostomum; PIWI proteins; piRNAs; stem cell maintenance; transposon silencing