A Transcriptomic Network Underlies Microstructural and Physiological Responses to Cadmium in Populus × canescens

Author:

He Jiali1,Li Hong1,Luo Jie1,Ma Chaofeng1,Li Shaojun1,Qu Long2,Gai Ying2,Jiang Xiangning2,Janz Dennis3,Polle Andrea3,Tyree Melvin1,Luo Zhi-Bin1

Affiliation:

1. College of Life Sciences and State Key Laboratory of Crop Stress Biology in Arid Areas (J.H., J.L., C.M., S.L., Z.-B.L.), Key Laboratory of Applied Entomology, College of Plant Protection (H.L.), and Key Laboratory of Environment and Ecology in Western China, Ministry of Education, College of Forestry (M.T., Z.-B.L.), Northwest A&F University, Yangling, Shaanxi 712100, China

2. National Engineering Laboratory of Tree Breeding, College of Life Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China (L.Q., Y.G., X.J.); and

3. Büsgen Institute, Department of Forest Botany and Tree Physiology, Georg-August University, 37077 Göttingen, Germany (D.J., A.P.)

Abstract

Abstract Bark tissue of Populus × canescens can hyperaccumulate cadmium, but microstructural, transcriptomic, and physiological response mechanisms are poorly understood. Histochemical assays, transmission electron microscopic observations, energy-dispersive x-ray microanalysis, and transcriptomic and physiological analyses have been performed to enhance our understanding of cadmium accumulation and detoxification in P. × canescens. Cadmium was allocated to the phloem of the bark, and subcellular cadmium compartmentalization occurred mainly in vacuoles of phloem cells. Transcripts involved in microstructural alteration, changes in nutrition and primary metabolism, and stimulation of stress responses showed significantly differential expression in the bark of P. × canescens exposed to cadmium. About 48% of the differentially regulated transcripts formed a coregulation network in which 43 hub genes played a central role both in cross talk among distinct biological processes and in coordinating the transcriptomic regulation in the bark of P. × canescens in response to cadmium. The cadmium transcriptome in the bark of P. × canescens was mirrored by physiological readouts. Cadmium accumulation led to decreased total nitrogen, phosphorus, and calcium and increased sulfur in the bark. Cadmium inhibited photosynthesis, resulting in decreased carbohydrate levels. Cadmium induced oxidative stress and antioxidants, including free proline, soluble phenolics, ascorbate, and thiol compounds. These results suggest that orchestrated microstructural, transcriptomic, and physiological regulation may sustain cadmium hyperaccumulation in P. × canescens bark and provide new insights into engineering woody plants for phytoremediation.

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Genetics,Physiology

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