Site-specific regulation of transcriptional responses to cadmium stress in the hyperaccumulator, Sedum alfredii: based on stem parenchymal and vascular cells
- 37 Downloads
We compared the transcriptomes of parenchymal and vascular cells of Sedum alfredii stem under Cd stress to reveal gene regulatory networks underlying Cd hyperaccumulation.
Cadmium (Cd) hyperaccumulation in plants is a complex biological process controlled by gene regulatory networks. Efficient transport through vascular systems and storage by parenchymal cells are vital for Cd hyperaccumulation in the Cd hyperaccumulator Sedum alfredii, but the genes involved are poorly understood. We investigated the spatial gene expression profiles of transport and storage sites in S. alfredii stem using laser-capture microdissection coupled with RNA sequencing. Gene expression patterns in response to Cd were distinct in vascular and parenchymal cells, indicating functional divisions that corresponded to Cd transportation and storage, respectively. In vascular cells, plasma membrane-related terms enriched a large number of differentially-expressed genes (DEGs) for foundational roles in Cd transportation. Parenchymal cells contained considerable DEGs specifically concentrated on vacuole-related terms associated with Cd sequestration and detoxification. In both cell types, DEGs were classified into different metabolic pathways in a similar way, indicating the role of Cd in activating a systemic stress signalling network where ATP-binding cassette transporters and Ca2+ signal pathways were probably involved. This study identified site-specific regulation of transcriptional responses to Cd stress in S. alfredii and analysed a collection of genes that possibly function in Cd transportation and detoxification, thus providing systemic information and direction for further investigation of Cd hyperaccumulation molecular mechanisms.
KeywordsCadmium Laser-capture microdissection RNA-seq Transporter Hyperaccumulation Signalling
The investigation of Cd distribution imaging by µ-XRF was conducted at the Advanced Photon Source, USA (Proposal No.: 23899) and we thank all the staff there. We also sincerely thank Vazyme Biotech (Nanjing, China) for their RNA sequencing service.
LL supervised and designed the experiments; YH and LX performed most of the experiments and analysed data with contributions from ST; YH and LL conceived the project and wrote the manuscript with contributions from XL and ST.
This work was supported by National Natural Science Foundation of China projects (31672235, 31471939), and the project from National Key Research and Development Program of China (2016YFD0800401).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no competing interests.
- Isaure MP, Huguet S, Meyer CL, Castillo-Michel H, Testemale D, Vantelon D, Saumitou-Laprade P, Verbruggen N, Sarret G (2015) Evidence of various mechanisms of Cd sequestration in the hyperaccumulator Arabidopsis halleri, the non-accumulator Arabidopsis lyrata, and their progenies by combined synchrotron-based techniques. J Exp Bot 66:3201–3214CrossRefGoogle Scholar
- Mendoza-Cozatl DG, Xie QQ, Akmakjian GZ, Jobe TO, Patel A, Stacey MG, Song LH, Demoin DW, Jurisson SS, Stacey G et al (2014) OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. Mol Plant 7:1455–1469CrossRefGoogle Scholar
- Nakazono M, Qiu F, Borsuk LA, Schnable PS (2003) Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15:583–596CrossRefGoogle Scholar
- Shi X, Sun HJ, Chen YT, Pan HW, Wang SF (2016) Transcriptome sequencing and expression analysis of cadmium (Cd) transport and detoxification related genes in Cd-accumulating Salix integra. Front Plant Sci 7:1577Google Scholar
- Vogel-Mikuš K, Simčič J, Pelicon P, Budnar M, Kump P, Nečemer M, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, Regvar M (2008) Comparison of essential and non-essential element distribution in leaves of the Cd/Zn hyperaccumulator Thlaspi praecox as revealed by micro-PIXE. Plant Cell Environ 31:1484–1496CrossRefGoogle Scholar
- Weber M, Harada E, Vess C, Roepenack-Lahaye EV, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281CrossRefGoogle Scholar
- Wojcik M, Vangronsveld J, D’Haen J, Tukiendorf A (2005) Cadmium tolerance in Thlaspi caerulescens-II. Localization of cadmium in Thlaspi caerulescens. Environ Exp Bot 53:163–171Google Scholar