Salt hypersensitivity is associated with excessive xylem development in a thermospermine‐deficient mutant of Arabidopsis thaliana

Abstract

In Arabidopsis, spermine is produced in most tissues and has been implicated in stress response, while its structural isomer thermospermine is only in xylem precursor cells. Studies on acaulis5 (acl5), a mutant defective in the biosynthesis of thermospermine, have revealed that thermospermine plays a repressive role in xylem development through enhancement of mRNA translation of the SAC51 family. In contrast, the pao5 mutant defective in the degradation of thermospermine has high levels of thermospermine and shows increased salt tolerance, suggesting a role of thermospermine in salt stress response. Here we compared acl5 with a mutant of spermine synthase, spms, in terms of abiotic stress tolerance and found that acl5 was much more sensitive to sodium than the wild-type and spms. A double-mutant of acl5 and sac51-d, which suppresses the excessive xylem phenotype of acl5, recovered normal sensitivity, while a quadruple T-DNA insertion mutant of the SAC51 family, which has an increased thermospermine level but shows excessive xylem development, showed increased salt sensitivity, unlike pao5. Together with the result that the salt tolerance of both wild-type and acl5 seedlings was improved by long-term treatment with thermospermine, we suggest a correlation of the salt tolerance with reduced xylem development rather than with the thermospermine level. We further found that the mutants containing high thermospermine levels showed increased tolerance to drought and heat stress, suggesting another role of thermospermine that may be common with that of spermine and secondary to that in restricting excess xylem development associated with salt hypersensitivity.

How roots and shoots communicate through stressful times

“…This may also explain the enhanced Lp r and drought resistance of the arabidopsis xnd1 mutants because a larger xylem area and an increased number of xylem vessels were observed in xnd1 mutants [16]. In response to salinity, mutants of ACAULIS5 (ACL5)encoding a putative spermine synthase required for xylem specificationexhibit higher salt accumulation and hypersensitivity to salt stress compared with WT plants [74], which is likely caused by excessive Na + loading via the root xylem owing to extra xylem vessels in the mutants [75,76].…”

“…TMO5 dimerizes with LONESOME HIGHWAY (LHW) to activate the expression of CK biosynthesis genes LOG3 and LOG4 which regulate periclinal cell divisions in (pro)cambium for secondary growth to produce new vasculature tissues [102]. Abiotic stress signaling pathways that are induced by drought, salinity, and ABA have shown an effect on the auxin-CKregulated vascular developmental pathways [68,69,74,84]. Transcriptome data mining of publicly available gene expression datasets reveals that various abiotic stresses can interfere with the expression of key regulators of vasculature development (Figure 2C), suggesting an impact of stress signaling on auxin-CK signaling to shape a functional vascular system to withstand various stress conditions.…”

“…During xylem development, drought-induced endodermal ABA signaling promotes miR165/166 and subsequently represses HD-ZIP IIIs[68,69]. Salt affects the auxin-CK feedback loop to regulate xylem development via ACL5 (see Box 1 in the main text)[74,105]. In phloem, several key pathways/regulators have been shown to be induced by drought, salt, and ABA signaling, including BRX, CLE peptide-BAM signaling, and the PEARs-SMXL3/4/5 module[81][82][83][84][85].…”

A Beginner’s Guide to Osmoprotection by Biostimulants

“…Thermospermine is synthesized by thermo-spermine synthase and is less well known than the other three polyamines. It has not been used as a treatment against stress, but its potential is worthy of mention because a thermospermine-deficient mutant is hypersensitive to salt in Arabidopsis thaliana [119].…”

Plant vascular development: mechanisms and environmental regulation

“…On the other hand, like drought, salt stress has been shown to reduce lumen in xylem vessels in Arabidopsis, tomato and Populus [124]. This reduction in overall xylem lumen development seems to be necessary to enhance salt tolerance, since the acl5 Arabidopsis mutants, with excessive, premature, xylem development, display salt hypersensitivity [125]. Several possible mechanisms may be responsible for this effect.…”