Phosphate-Starvation-Inducible S-Like RNase Genes in Rice Are Involved in Phosphate Source Recycling by RNA Decay

The fine-tuning of inorganic phosphate (Pi) for enhanced use efficiency has long been a challenging subject in agriculture, particularly in regard to rice as a major crop plant. Among ribonucleases (RNases), the RNase T2 family is broadly distributed across kingdoms, but little has been known on its...

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Main Authors: Yun-Shil Gho, Heebak Choi, Sunok Moon, Min Yeong Song, Ha Eun Park, Doh-Hoon Kim, Sun-Hwa Ha, Ki-Hong Jung
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2020.585561/full
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author Yun-Shil Gho
Heebak Choi
Sunok Moon
Min Yeong Song
Ha Eun Park
Doh-Hoon Kim
Sun-Hwa Ha
Ki-Hong Jung
author_facet Yun-Shil Gho
Heebak Choi
Sunok Moon
Min Yeong Song
Ha Eun Park
Doh-Hoon Kim
Sun-Hwa Ha
Ki-Hong Jung
author_sort Yun-Shil Gho
collection DOAJ
description The fine-tuning of inorganic phosphate (Pi) for enhanced use efficiency has long been a challenging subject in agriculture, particularly in regard to rice as a major crop plant. Among ribonucleases (RNases), the RNase T2 family is broadly distributed across kingdoms, but little has been known on its substrate specificity compared to RNase A and RNase T1 families. Class I and class II of the RNase T2 family are defined as the S-like RNase (RNS) family and have showed the connection to Pi recycling in Arabidopsis. In this study, we first carried out a phylogenetic analysis of eight rice and five Arabidopsis RNS genes and identified mono-specific class I and dicot-specific class I RNS genes, suggesting the possibility of functional diversity between class I RNS family members in monocot and dicot species through evolution. We then compared the in silico expression patterns of all RNS genes in rice and Arabidopsis under normal and Pi-deficient conditions and further confirmed the expression patterns of rice RNS genes via qRT-PCR analysis. Subsequently, we found that most of the OsRNS genes were differentially regulated under Pi-deficient treatment. Association of Pi recycling by RNase activity in rice was confirmed by measuring total RNA concentration and ribonuclease activity of shoot and root samples under Pi-sufficient or Pi-deficient treatment during 21 days. The total RNA concentrations were decreased by < 60% in shoots and < 80% in roots under Pi starvation, respectively, while ribonuclease activity increased correspondingly. We further elucidate the signaling pathway of Pi starvation through upregulation of the OsRNS genes. The 2-kb promoter region of all OsRNS genes with inducible expression patterns under Pi deficiency contains a high frequency of P1BS cis-acting regulatory element (CRE) known as the OsPHR2 binding site, suggesting that the OsRNS family is likely to be controlled by OsPHR2. Finally, the dynamic transcriptional regulation of OsRNS genes by overexpression of OsPHR2, ospho2 mutant, and overexpression of OsPT1 lines involved in Pi signaling pathway suggests the molecular basis of OsRNS family in Pi recycling via RNA decay under Pi starvation.
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spelling doaj.art-ddda9a486e7346a59c86b6cb08350cfb2022-12-21T20:29:57ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-11-011110.3389/fpls.2020.585561585561Phosphate-Starvation-Inducible S-Like RNase Genes in Rice Are Involved in Phosphate Source Recycling by RNA DecayYun-Shil Gho0Heebak Choi1Sunok Moon2Min Yeong Song3Ha Eun Park4Doh-Hoon Kim5Sun-Hwa Ha6Ki-Hong Jung7Graduate School of Biotechnology, Kyung Hee University, Yongin, South KoreaGraduate School of Biotechnology, Kyung Hee University, Yongin, South KoreaGraduate School of Biotechnology, Kyung Hee University, Yongin, South KoreaGraduate School of Biotechnology, Kyung Hee University, Yongin, South KoreaGraduate School of Biotechnology, Kyung Hee University, Yongin, South KoreaDepartment of Life Science, College of Life Science and Natural Resources, Dong-A University, Busan, South KoreaGraduate School of Biotechnology, Kyung Hee University, Yongin, South KoreaGraduate School of Biotechnology, Kyung Hee University, Yongin, South KoreaThe fine-tuning of inorganic phosphate (Pi) for enhanced use efficiency has long been a challenging subject in agriculture, particularly in regard to rice as a major crop plant. Among ribonucleases (RNases), the RNase T2 family is broadly distributed across kingdoms, but little has been known on its substrate specificity compared to RNase A and RNase T1 families. Class I and class II of the RNase T2 family are defined as the S-like RNase (RNS) family and have showed the connection to Pi recycling in Arabidopsis. In this study, we first carried out a phylogenetic analysis of eight rice and five Arabidopsis RNS genes and identified mono-specific class I and dicot-specific class I RNS genes, suggesting the possibility of functional diversity between class I RNS family members in monocot and dicot species through evolution. We then compared the in silico expression patterns of all RNS genes in rice and Arabidopsis under normal and Pi-deficient conditions and further confirmed the expression patterns of rice RNS genes via qRT-PCR analysis. Subsequently, we found that most of the OsRNS genes were differentially regulated under Pi-deficient treatment. Association of Pi recycling by RNase activity in rice was confirmed by measuring total RNA concentration and ribonuclease activity of shoot and root samples under Pi-sufficient or Pi-deficient treatment during 21 days. The total RNA concentrations were decreased by < 60% in shoots and < 80% in roots under Pi starvation, respectively, while ribonuclease activity increased correspondingly. We further elucidate the signaling pathway of Pi starvation through upregulation of the OsRNS genes. The 2-kb promoter region of all OsRNS genes with inducible expression patterns under Pi deficiency contains a high frequency of P1BS cis-acting regulatory element (CRE) known as the OsPHR2 binding site, suggesting that the OsRNS family is likely to be controlled by OsPHR2. Finally, the dynamic transcriptional regulation of OsRNS genes by overexpression of OsPHR2, ospho2 mutant, and overexpression of OsPT1 lines involved in Pi signaling pathway suggests the molecular basis of OsRNS family in Pi recycling via RNA decay under Pi starvation.https://www.frontiersin.org/articles/10.3389/fpls.2020.585561/fullriceS-like RNasesphosphate starvationphosphate recyclingRNA degradation
spellingShingle Yun-Shil Gho
Heebak Choi
Sunok Moon
Min Yeong Song
Ha Eun Park
Doh-Hoon Kim
Sun-Hwa Ha
Ki-Hong Jung
Phosphate-Starvation-Inducible S-Like RNase Genes in Rice Are Involved in Phosphate Source Recycling by RNA Decay
Frontiers in Plant Science
rice
S-like RNases
phosphate starvation
phosphate recycling
RNA degradation
title Phosphate-Starvation-Inducible S-Like RNase Genes in Rice Are Involved in Phosphate Source Recycling by RNA Decay
title_full Phosphate-Starvation-Inducible S-Like RNase Genes in Rice Are Involved in Phosphate Source Recycling by RNA Decay
title_fullStr Phosphate-Starvation-Inducible S-Like RNase Genes in Rice Are Involved in Phosphate Source Recycling by RNA Decay
title_full_unstemmed Phosphate-Starvation-Inducible S-Like RNase Genes in Rice Are Involved in Phosphate Source Recycling by RNA Decay
title_short Phosphate-Starvation-Inducible S-Like RNase Genes in Rice Are Involved in Phosphate Source Recycling by RNA Decay
title_sort phosphate starvation inducible s like rnase genes in rice are involved in phosphate source recycling by rna decay
topic rice
S-like RNases
phosphate starvation
phosphate recycling
RNA degradation
url https://www.frontiersin.org/articles/10.3389/fpls.2020.585561/full
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