Populus euphratica GRP2 Interacts with Target mRNAs to Negatively Regulate Salt Tolerance by Interfering with Photosynthesis, Na+, and ROS Homeostasis

Li, Jing; Zhao, Rui; Liu, Jian; Yao, Jun; Ma, Siyuan; Yin, Kexin; Zhang, Ying; Liu, Zhe; Yan, Caixia; Zhao, Nan; Zhou, Xiaoyang; Chen, Shaoliang

doi:10.3390/ijms25042046

Open AccessArticle

Populus euphratica GRP2 Interacts with Target mRNAs to Negatively Regulate Salt Tolerance by Interfering with Photosynthesis, Na⁺, and ROS Homeostasis

by

Jing Li

^1,†,

Rui Zhao

^1,†,

Jian Liu

¹,

Jun Yao

²,

Siyuan Ma

¹,

Kexin Yin

¹,

Ying Zhang

¹,

Zhe Liu

¹,

Caixia Yan

¹,

Nan Zhao

¹,

Xiaoyang Zhou

¹ and

Shaoliang Chen

^1,*

¹

State Key Laboratory of Efficient Production of Forest Resources, College of Biological Science and Technology, Beijing Forestry University, Beijing 100083, China

²

Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou 510520, China

^*

Author to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Int. J. Mol. Sci. 2024, 25(4), 2046; https://doi.org/10.3390/ijms25042046

Submission received: 18 December 2023 / Revised: 17 January 2024 / Accepted: 6 February 2024 / Published: 7 February 2024

(This article belongs to the Special Issue Plant Response to Abiotic Stress 2.0)

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Abstract

The transcription of glycine-rich RNA-binding protein 2 (PeGRP2) transiently increased in the roots and shoots of Populus euphratica (a salt-resistant poplar) upon initial salt exposure and tended to decrease after long-term NaCl stress (100 mM, 12 days). PeGRP2 overexpression in the hybrid Populus tremula × P. alba ‘717-1B4’ (P. × canescens) increased its salt sensitivity, which was reflected in the plant’s growth and photosynthesis. PeGRP2 contains a conserved RNA recognition motif domain at the N-terminus, and RNA affinity purification (RAP) sequencing was developed to enrich the target mRNAs that physically interacted with PeGRP2 in P. × canescens. RAP sequencing combined with RT-qPCR revealed that NaCl decreased the transcripts of PeGRP2-interacting mRNAs encoding photosynthetic proteins, antioxidative enzymes, ATPases, and Na⁺/H⁺ antiporters in this transgenic poplar. Specifically, PeGRP2 negatively affected the stability of the target mRNAs encoding the photosynthetic proteins PETC and RBCMT; antioxidant enzymes SOD[Mn], CDSP32, and CYB1-2; ATPases AHA11, ACA8, and ACA9; and the Na⁺/H⁺ antiporter NHA1. This resulted in (i) a greater reduction in Fv/Fm, YII, ETR, and Pn; (ii) less pronounced activation of antioxidative enzymes; and (iii) a reduced ability to maintain Na⁺ homeostasis in the transgenic poplars during long-term salt stress, leading to their lowered ability to tolerate salinity stress.

Keywords: glycine-rich RNA-binding protein; RNA affinity purification sequencing; Na⁺ flux; ROS; antioxidant enzyme; photosynthesis; ATPase

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MDPI and ACS Style

Li, J.; Zhao, R.; Liu, J.; Yao, J.; Ma, S.; Yin, K.; Zhang, Y.; Liu, Z.; Yan, C.; Zhao, N.; et al. Populus euphratica GRP2 Interacts with Target mRNAs to Negatively Regulate Salt Tolerance by Interfering with Photosynthesis, Na⁺, and ROS Homeostasis. Int. J. Mol. Sci. 2024, 25, 2046. https://doi.org/10.3390/ijms25042046

AMA Style

Li J, Zhao R, Liu J, Yao J, Ma S, Yin K, Zhang Y, Liu Z, Yan C, Zhao N, et al. Populus euphratica GRP2 Interacts with Target mRNAs to Negatively Regulate Salt Tolerance by Interfering with Photosynthesis, Na⁺, and ROS Homeostasis. International Journal of Molecular Sciences. 2024; 25(4):2046. https://doi.org/10.3390/ijms25042046

Chicago/Turabian Style

Li, Jing, Rui Zhao, Jian Liu, Jun Yao, Siyuan Ma, Kexin Yin, Ying Zhang, Zhe Liu, Caixia Yan, Nan Zhao, and et al. 2024. "Populus euphratica GRP2 Interacts with Target mRNAs to Negatively Regulate Salt Tolerance by Interfering with Photosynthesis, Na⁺, and ROS Homeostasis" International Journal of Molecular Sciences 25, no. 4: 2046. https://doi.org/10.3390/ijms25042046

APA Style

Li, J., Zhao, R., Liu, J., Yao, J., Ma, S., Yin, K., Zhang, Y., Liu, Z., Yan, C., Zhao, N., Zhou, X., & Chen, S. (2024). Populus euphratica GRP2 Interacts with Target mRNAs to Negatively Regulate Salt Tolerance by Interfering with Photosynthesis, Na⁺, and ROS Homeostasis. International Journal of Molecular Sciences, 25(4), 2046. https://doi.org/10.3390/ijms25042046

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Populus euphratica GRP2 Interacts with Target mRNAs to Negatively Regulate Salt Tolerance by Interfering with Photosynthesis, Na⁺, and ROS Homeostasis

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