Constitutive expression of arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in tomato confers auxin-independent hypocotyl elongation

Angela K. Spartz, Vai S. Lor, Hong Ren, Neil E. Olszewski, Nathan D. Miller, Guosheng Wu, Edgar P. Spalding, William M. Gray

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

The plant hormone indole-3-acetic acid (IAA or auxin) mediates the elongation growth of shoot tissues by promoting cell expansion. According to the acid growth theory proposed in the 1970s, auxin activates plasma membrane H+-ATPases (PM H+- ATPases) to facilitate cell expansion by both loosening the cell wall through acidification and promoting solute uptake. Mechanistically, however, this process is poorly understood. Recent findings in Arabidopsis (Arabidopsis thaliana) have demonstrated that auxin-induced SMALL AUXIN UP RNA (SAUR) genes promote elongation growth and play a key role in PM H+-ATPase activation by inhibiting PP2C.D family protein phosphatases. Here, we extend these findings by demonstrating that SAUR proteins also inhibit tomato PP2C.D family phosphatases and that AtSAUR19 overexpression in tomato (Solanum lycopersicum) confers the same suite of phenotypes as previously reported for Arabidopsis. Furthermore, we employ a custom image-based method for measuring hypocotyl segment elongation with high resolution and a method for measuring cell wall mechanical properties, to add mechanistic details to the emerging description of auxin-mediated cell expansion. We find that constitutive expression of GFP-AtSAUR19 bypasses the normal requirement of auxin for elongation growth by increasing the mechanical extensibility of excised hypocotyl segments. In contrast, hypocotyl segments overexpressing a PP2C.D phosphatase are specifically impaired in auxin-mediated elongation. The time courses of auxin-induced SAUR expression and auxindependent elongation growth were closely correlated. These findings indicate that induction of SAUR expression is sufficient to elicit auxin-mediated expansion growth by activating PM H+-ATPases to facilitate apoplast acidification and mechanical wall loosening.

Original languageEnglish (US)
Pages (from-to)1453-1462
Number of pages10
JournalPlant Physiology
Volume173
Issue number2
DOIs
StatePublished - Feb 2017

Fingerprint

Hypocotyl
Indoleacetic Acids
Lycopersicon esculentum
Arabidopsis
hypocotyls
auxins
tomatoes
Growth
RNA
H-transporting ATP synthase
Proton-Translocating ATPases
Phosphoric Monoester Hydrolases
indole acetic acid
Cell Wall
acidification
cell walls
Plant Growth Regulators
extensibility
Phosphoprotein Phosphatases
apoplast

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural

Cite this

Constitutive expression of arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in tomato confers auxin-independent hypocotyl elongation. / Spartz, Angela K.; Lor, Vai S.; Ren, Hong; Olszewski, Neil E.; Miller, Nathan D.; Wu, Guosheng; Spalding, Edgar P.; Gray, William M.

In: Plant Physiology, Vol. 173, No. 2, 02.2017, p. 1453-1462.

Research output: Contribution to journalArticle

@article{f263f0b558234d5fa085b4928f77565c,
title = "Constitutive expression of arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in tomato confers auxin-independent hypocotyl elongation",
abstract = "The plant hormone indole-3-acetic acid (IAA or auxin) mediates the elongation growth of shoot tissues by promoting cell expansion. According to the acid growth theory proposed in the 1970s, auxin activates plasma membrane H+-ATPases (PM H+- ATPases) to facilitate cell expansion by both loosening the cell wall through acidification and promoting solute uptake. Mechanistically, however, this process is poorly understood. Recent findings in Arabidopsis (Arabidopsis thaliana) have demonstrated that auxin-induced SMALL AUXIN UP RNA (SAUR) genes promote elongation growth and play a key role in PM H+-ATPase activation by inhibiting PP2C.D family protein phosphatases. Here, we extend these findings by demonstrating that SAUR proteins also inhibit tomato PP2C.D family phosphatases and that AtSAUR19 overexpression in tomato (Solanum lycopersicum) confers the same suite of phenotypes as previously reported for Arabidopsis. Furthermore, we employ a custom image-based method for measuring hypocotyl segment elongation with high resolution and a method for measuring cell wall mechanical properties, to add mechanistic details to the emerging description of auxin-mediated cell expansion. We find that constitutive expression of GFP-AtSAUR19 bypasses the normal requirement of auxin for elongation growth by increasing the mechanical extensibility of excised hypocotyl segments. In contrast, hypocotyl segments overexpressing a PP2C.D phosphatase are specifically impaired in auxin-mediated elongation. The time courses of auxin-induced SAUR expression and auxindependent elongation growth were closely correlated. These findings indicate that induction of SAUR expression is sufficient to elicit auxin-mediated expansion growth by activating PM H+-ATPases to facilitate apoplast acidification and mechanical wall loosening.",
author = "Spartz, {Angela K.} and Lor, {Vai S.} and Hong Ren and Olszewski, {Neil E.} and Miller, {Nathan D.} and Guosheng Wu and Spalding, {Edgar P.} and Gray, {William M.}",
year = "2017",
month = "2",
doi = "10.1104/pp.16.01514",
language = "English (US)",
volume = "173",
pages = "1453--1462",
journal = "Plant Physiology",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "2",

}

TY - JOUR

T1 - Constitutive expression of arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in tomato confers auxin-independent hypocotyl elongation

AU - Spartz, Angela K.

AU - Lor, Vai S.

AU - Ren, Hong

AU - Olszewski, Neil E.

AU - Miller, Nathan D.

AU - Wu, Guosheng

AU - Spalding, Edgar P.

AU - Gray, William M.

PY - 2017/2

Y1 - 2017/2

N2 - The plant hormone indole-3-acetic acid (IAA or auxin) mediates the elongation growth of shoot tissues by promoting cell expansion. According to the acid growth theory proposed in the 1970s, auxin activates plasma membrane H+-ATPases (PM H+- ATPases) to facilitate cell expansion by both loosening the cell wall through acidification and promoting solute uptake. Mechanistically, however, this process is poorly understood. Recent findings in Arabidopsis (Arabidopsis thaliana) have demonstrated that auxin-induced SMALL AUXIN UP RNA (SAUR) genes promote elongation growth and play a key role in PM H+-ATPase activation by inhibiting PP2C.D family protein phosphatases. Here, we extend these findings by demonstrating that SAUR proteins also inhibit tomato PP2C.D family phosphatases and that AtSAUR19 overexpression in tomato (Solanum lycopersicum) confers the same suite of phenotypes as previously reported for Arabidopsis. Furthermore, we employ a custom image-based method for measuring hypocotyl segment elongation with high resolution and a method for measuring cell wall mechanical properties, to add mechanistic details to the emerging description of auxin-mediated cell expansion. We find that constitutive expression of GFP-AtSAUR19 bypasses the normal requirement of auxin for elongation growth by increasing the mechanical extensibility of excised hypocotyl segments. In contrast, hypocotyl segments overexpressing a PP2C.D phosphatase are specifically impaired in auxin-mediated elongation. The time courses of auxin-induced SAUR expression and auxindependent elongation growth were closely correlated. These findings indicate that induction of SAUR expression is sufficient to elicit auxin-mediated expansion growth by activating PM H+-ATPases to facilitate apoplast acidification and mechanical wall loosening.

AB - The plant hormone indole-3-acetic acid (IAA or auxin) mediates the elongation growth of shoot tissues by promoting cell expansion. According to the acid growth theory proposed in the 1970s, auxin activates plasma membrane H+-ATPases (PM H+- ATPases) to facilitate cell expansion by both loosening the cell wall through acidification and promoting solute uptake. Mechanistically, however, this process is poorly understood. Recent findings in Arabidopsis (Arabidopsis thaliana) have demonstrated that auxin-induced SMALL AUXIN UP RNA (SAUR) genes promote elongation growth and play a key role in PM H+-ATPase activation by inhibiting PP2C.D family protein phosphatases. Here, we extend these findings by demonstrating that SAUR proteins also inhibit tomato PP2C.D family phosphatases and that AtSAUR19 overexpression in tomato (Solanum lycopersicum) confers the same suite of phenotypes as previously reported for Arabidopsis. Furthermore, we employ a custom image-based method for measuring hypocotyl segment elongation with high resolution and a method for measuring cell wall mechanical properties, to add mechanistic details to the emerging description of auxin-mediated cell expansion. We find that constitutive expression of GFP-AtSAUR19 bypasses the normal requirement of auxin for elongation growth by increasing the mechanical extensibility of excised hypocotyl segments. In contrast, hypocotyl segments overexpressing a PP2C.D phosphatase are specifically impaired in auxin-mediated elongation. The time courses of auxin-induced SAUR expression and auxindependent elongation growth were closely correlated. These findings indicate that induction of SAUR expression is sufficient to elicit auxin-mediated expansion growth by activating PM H+-ATPases to facilitate apoplast acidification and mechanical wall loosening.

UR - http://www.scopus.com/inward/record.url?scp=85011411835&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85011411835&partnerID=8YFLogxK

U2 - 10.1104/pp.16.01514

DO - 10.1104/pp.16.01514

M3 - Article

C2 - 27999086

AN - SCOPUS:85011411835

VL - 173

SP - 1453

EP - 1462

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 2

ER -