Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) Breit
Nowadays, because of the great benefit to human health, more and more efforts have been made to increase the production of alkaloids in Pinellia ternata (Thunb.) Breit. Phosphate (Pi) plays a critical role in plant growth and development, as well as secondary metabolism. However, its effect and regu...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-08-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.914648/full |
| _version_ | 1797680771431923712 |
|---|---|
| author | Huihui Wang Huihui Wang Jitao Hu Jitao Hu Linying Li Xueying Zhang Hao Zhang Zongsuo Liang Qing Sheng Yuqing He Gaojie Hong |
| author_facet | Huihui Wang Huihui Wang Jitao Hu Jitao Hu Linying Li Xueying Zhang Hao Zhang Zongsuo Liang Qing Sheng Yuqing He Gaojie Hong |
| author_sort | Huihui Wang |
| collection | DOAJ |
| description | Nowadays, because of the great benefit to human health, more and more efforts have been made to increase the production of alkaloids in Pinellia ternata (Thunb.) Breit. Phosphate (Pi) plays a critical role in plant growth and development, as well as secondary metabolism. However, its effect and regulation mechanism of Pi signaling on alkaloid biosynthesis call for further exploration. Here, we reported that Pi starvation could induce alkaloid accumulation in P. ternata. We cloned a cDNA sequence encoding PtPHR1 from P. ternata, which was further identified by nuclear localization, transcription activity, and binding ability to the PHR1-binding sequence. We found that the transformation of PtPHR1 into the Arabidopsis phr1 mutant (designated as PtPHR1OE/phr1) led to the rescue of the phenotype of the phr1 mutant to that of the wild-type, including the expression level of Pi starvation-induced genes and anthocyanin accumulation. The combination of these biochemical and genetic experiments indicated that PtPHR1 was intended to have a role similar to that of AtPHR1 in Pi signaling and metabolic responses. Interestingly, we found that Pi starvation also induced the production of benzoic acid, an intermediate in the biosynthetic pathway of phenylpropylamino alkaloids. Furthermore, this induction effect was impaired in the phr1 mutant but partly recovered in PtPHR1OE/phr1 plants. Together, our data suggest that Pi starvation promoted benzoic acid-derived alkaloid biosynthesis in P. ternata under the control of PtPHR1. Our finding that PtPHR1 is involved in the regulation of Pi signaling on alkaloid biosynthesis shows a direct link between the Pi nutrient supply and secondary metabolism. |
| first_indexed | 2024-03-11T23:35:02Z |
| format | Article |
| id | doaj.art-906dc3b537e449579df41f17bb82d142 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-03-11T23:35:02Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-906dc3b537e449579df41f17bb82d1422023-09-20T04:54:26ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-08-011310.3389/fpls.2022.914648914648Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) BreitHuihui Wang0Huihui Wang1Jitao Hu2Jitao Hu3Linying Li4Xueying Zhang5Hao Zhang6Zongsuo Liang7Qing Sheng8Yuqing He9Gaojie Hong10College of Life Sciences, Zhejiang Sci-Tech University, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaCollege of Life Sciences, Zhejiang Sci-Tech University, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaCollege of Pharmacy, Zhejiang Chinese Medical University, Hangzhou, ChinaCollege of Life Sciences, Zhejiang Sci-Tech University, Hangzhou, ChinaCollege of Life Sciences, Zhejiang Sci-Tech University, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaNowadays, because of the great benefit to human health, more and more efforts have been made to increase the production of alkaloids in Pinellia ternata (Thunb.) Breit. Phosphate (Pi) plays a critical role in plant growth and development, as well as secondary metabolism. However, its effect and regulation mechanism of Pi signaling on alkaloid biosynthesis call for further exploration. Here, we reported that Pi starvation could induce alkaloid accumulation in P. ternata. We cloned a cDNA sequence encoding PtPHR1 from P. ternata, which was further identified by nuclear localization, transcription activity, and binding ability to the PHR1-binding sequence. We found that the transformation of PtPHR1 into the Arabidopsis phr1 mutant (designated as PtPHR1OE/phr1) led to the rescue of the phenotype of the phr1 mutant to that of the wild-type, including the expression level of Pi starvation-induced genes and anthocyanin accumulation. The combination of these biochemical and genetic experiments indicated that PtPHR1 was intended to have a role similar to that of AtPHR1 in Pi signaling and metabolic responses. Interestingly, we found that Pi starvation also induced the production of benzoic acid, an intermediate in the biosynthetic pathway of phenylpropylamino alkaloids. Furthermore, this induction effect was impaired in the phr1 mutant but partly recovered in PtPHR1OE/phr1 plants. Together, our data suggest that Pi starvation promoted benzoic acid-derived alkaloid biosynthesis in P. ternata under the control of PtPHR1. Our finding that PtPHR1 is involved in the regulation of Pi signaling on alkaloid biosynthesis shows a direct link between the Pi nutrient supply and secondary metabolism.https://www.frontiersin.org/articles/10.3389/fpls.2022.914648/fullPinellia ternata (Thunb.) Beritalkaloid metabolismbenzoic acid (BA)phosphate signalingPtPHR1 |
| spellingShingle | Huihui Wang Huihui Wang Jitao Hu Jitao Hu Linying Li Xueying Zhang Hao Zhang Zongsuo Liang Qing Sheng Yuqing He Gaojie Hong Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) Breit Frontiers in Plant Science Pinellia ternata (Thunb.) Berit alkaloid metabolism benzoic acid (BA) phosphate signaling PtPHR1 |
| title | Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) Breit |
| title_full | Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) Breit |
| title_fullStr | Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) Breit |
| title_full_unstemmed | Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) Breit |
| title_short | Involvement of PtPHR1 in phosphates starvation-induced alkaloid biosynthesis in Pinellia ternata (Thunb.) Breit |
| title_sort | involvement of ptphr1 in phosphates starvation induced alkaloid biosynthesis in pinellia ternata thunb breit |
| topic | Pinellia ternata (Thunb.) Berit alkaloid metabolism benzoic acid (BA) phosphate signaling PtPHR1 |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.914648/full |
| work_keys_str_mv | AT huihuiwang involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT huihuiwang involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT jitaohu involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT jitaohu involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT linyingli involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT xueyingzhang involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT haozhang involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT zongsuoliang involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT qingsheng involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT yuqinghe involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit AT gaojiehong involvementofptphr1inphosphatesstarvationinducedalkaloidbiosynthesisinpinelliaternatathunbbreit |