Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance

Xiao Fang Zhu, Guijie Lei, Zhi Wei Wang, Yuan Zhi Shi, Janet Braam, Gui Xin Li, Shao Jian Zheng

Research output: Contribution to journalArticle

47 Citations (Scopus)

Abstract

Whether aluminum toxicity is an apoplastic or symplastic phenomenon is still a matter of debate. Here, we found that three auxin overproducing mutants, yucca, the recessive mutant superroot2, and superroot1 had increased aluminum sensitivity, while a transfer DNA insertion mutant, xyloglucan endotransglucosylase/hydrolases15 (xth15), showed enhanced aluminum resistance, accompanied by low endogenous indole-3-acetic acid levels, implying that auxin may be involved in plant responses to aluminum stress. We used yucca and xth15 mutants for further study. The two mutants accumulated similar total aluminum in roots and had significantly reduced cell wall aluminum and increased symplastic aluminum content relative to the wild-type ecotype Columbia, indicating that altered aluminum levels in the symplast or cell wall cannot fully explain the differential aluminum resistance of these two mutants. The expression of Al sensitive1 (ALS1), a gene that functions in aluminum redistribution between the cytoplasm and vacuole and contributes to symplastic aluminum detoxification, was less abundant in yucca and more abundant in xth15 than the wild type, consistent with possible ALS1 function conferring altered aluminum sensitivity in the two mutants. Consistent with the idea that xth15 can tolerate more symplastic aluminum because of possible ALS1 targeting to the vacuole, morin staining of yucca root tip sections showed more aluminum accumulation in the cytosol than in the wild type, and xth15 showed reduced morin staining of cytosolic aluminum, even though yucca and xth15 had similar overall symplastic aluminum content. Exogenous application of an active auxin analog, naphthylacetic acid, to the wild type mimicked the aluminum sensitivity and distribution phenotypes of yucca, verifying that auxin may regulate aluminum distribution in cells. Together, these data demonstrate that auxin negatively regulates aluminum tolerance through altering ALS1 expression and aluminum distribution within plant cells, and plants must coordinate exclusion and internal detoxification to reduce aluminum toxicity effectively.

Original languageEnglish
Pages (from-to)1947-1955
Number of pages9
JournalPlant Physiology
Volume162
Issue number4
DOIs
Publication statusPublished - Aug 1 2013
Externally publishedYes

Fingerprint

Aluminum
aluminum
xyloglucan - xyloglucosyltransferase
Yucca
xyloglucan:xyloglucosyl transferase
Indoleacetic Acids
mutants
auxins
Vacuoles
Cell Wall
vacuoles
cell walls
Staining and Labeling
Ecotype
toxicity
transfer DNA
symplast
Meristem
Plant Cells

ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

Cite this

Zhu, X. F., Lei, G., Wang, Z. W., Shi, Y. Z., Braam, J., Li, G. X., & Zheng, S. J. (2013). Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. Plant Physiology, 162(4), 1947-1955. https://doi.org/10.1104/pp.113.219147

Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. / Zhu, Xiao Fang; Lei, Guijie; Wang, Zhi Wei; Shi, Yuan Zhi; Braam, Janet; Li, Gui Xin; Zheng, Shao Jian.

In: Plant Physiology, Vol. 162, No. 4, 01.08.2013, p. 1947-1955.

Research output: Contribution to journalArticle

Zhu, Xiao Fang ; Lei, Guijie ; Wang, Zhi Wei ; Shi, Yuan Zhi ; Braam, Janet ; Li, Gui Xin ; Zheng, Shao Jian. / Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. In: Plant Physiology. 2013 ; Vol. 162, No. 4. pp. 1947-1955.
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