Abstract

Drought severely limits plant development and growth; accordingly, plants have evolved strategies to prevent water loss and adapt to water deficit conditions. However, experimental cases that corroborate these evolutionary processes are limited. The LACCASEs (LACs) family is involved in various plant development and growth processes. Here, we performed an evolutionary analysis of LACs from Populus euphratica and characterized the functions of LACs in Arabidopsis and poplar. The results showed that in PeuLACs, multiple gene duplications led to apparent functional redundancy as the result of various selective pressures. Among them, PeuLAC2 underwent strong positive selection. Heterologous expression analyses showed that the overexpression of PeuLAC2 alters the xylem structure of plants, including thickening the secondary cell wall (SCW) and increasing the fiber cell length and stem tensile strength. Altogether, these changes improve the water transport capacity of plants. The analysis of the physiological experimental results showed that PeuLAC2-OE lines exhibited a stronger antioxidant response and greater drought tolerance than WT. Three genes screened by transcriptome analysis, NAC025, BG1, and UGT, that are associated with SCW synthesis and drought stress were all upregulated in the PeuLAC2-OE lines, implying that the overexpression of PeuLAC2 thickened the SCW, improved the water transport capacity of the plant, and further enhanced its drought tolerance. Our study highlights that genes that have undergone adaptive evolution may participate in the development of adaptive traits in P. euphratica and that PeuLAC2 could be a candidate gene for molecular genetic breeding in trees.

Highlights

  • Water is one of the foremost limiting factors for normal plant survival

  • Identification of LAC genes from the P. euphratica genome We identified the LAC family through a BLASTp search using 17 Arabidopsis LAC protein sequences to BLAST against the P. euphratica genome

  • To investigate whether PeuLAC2 is involved in drought-induced oxidative stress, we examined the related parameters in PeuLAC2-OE and WT Arabidopsis plants treated by withholding water for 0, 12, and 15 days

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Summary

Introduction

Water is one of the foremost limiting factors for normal plant survival. Plants, especially those distributed in arid and semiarid regions, have evolved various strategies to prevent water loss or adapt to growth in conditions with water deficiency[1]. In Arabidopsis, a total of 17 LAC members have been identified[12], four of which (LAC4, LAC11, LAC15, and LAC17) are involved in lignin biosynthesis and regulating cell wall structure[11,13,14]. The overexpression of GhLAC15 enhances resistance to Verticillium wilt by increasing lignification and lignin content in plant cell walls[21]. The secondary cell wall (SCW) provides mechanical support for plants[30] and acts as a defense barrier to pathogen and insect attacks[31,32] and provides a channel for the long-distance transportation of nutrients and water. With the polymorphisms in leaves, these traits allow the plants to exhibit physiological responses that help them adapt to extremely arid environments, including decreased photosynthetic activity, stomatal aperture control, and altered cell wall elasticity[33]. Our study provides insights into the adaptive evolution of key genes that provide important genetic resources for the adaptation of desert poplar to extremely arid environments

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PeuLAC1
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