Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis

Abstract

Arbuscular mycorrhizal (AM) symbiosis can enhance plant resistance to NaCl stress in several ways. Two fundamental roles involve osmotic and ionic adjustment. By stimulating accumulation of solutes, the symbiosis can help plants sustain optimal water balance and diminish Na(+) toxicity. The size of the AM effect on osmolytes has varied widely and is unpredictable. We conducted a meta-analysis to determine the size of the AM effect on 22 plant solute characteristics after exposure to NaCl and to examine how experimental conditions have influenced the AM effect. Viewed across studies, AM symbioses have had marked effects on plant K(+), increasing root and shoot K(+) concentrations by an average of 47 and 42%, respectively, and root and shoot K(+)/Na(+) ratios by 47 and 58%, respectively. Among organic solutes, soluble carbohydrates have been most impacted, with AM-induced increases of 28 and 19% in shoots and roots. The symbiosis has had no consistent effect on several characteristics, including root glycine betaine concentration, root or shoot Cl(-) concentrations, leaf Ψπ, or shoot proline or polyamine concentrations. The AM effect has been very small for shoot Ca(++) concentration and root concentrations of Na(+), Mg(++) and proline. Interpretations about AM-conferred benefits regarding these compounds may be best gauged within the context of the individual studies. Shoot and root K(+)/Na(+) ratios and root proline concentration showed significant between-study heterogeneity, and we examined nine moderator variables to explore what might explain the differences in mycorrhizal effects on these parameters. Moderators with significant impacts included AM taxa, host type, presence or absence of AM growth promotion, stress severity, and whether NaCl constituted part or all of the experimental saline stress treatment. Meta-regression of shoot K(+)/Na(+) ratio showed a positive response to root colonization, and root K(+)/Na(+) ratio a negative response to time of exposure to NaCl.

Keywords: K+/Na+ ratio; NaCl stress; arbuscular mycorrhiza; compatible solutes; meta-analysis; osmotic adjustment; salinity; salt stress.

Figure 1

Weighted summary effect sizes (ln R) and 95% bootstrapped confidence intervals (CIs) for AM effect on plants exposed to NaCl stress (A) and unstressed controls (B). p ≤ 0.05 indicates that the moderator level was significantly different than zero. The absent forest plot for leaf Ψ_π in (B) reflects insufficient studies to have included that moderator level in the meta-analysis.

Figure 2

Weighted summary effect sizes (ln R) and 95% bootstrapped confidence intervals (CIs) for influence of NaCl stress on shoot K⁺/Na⁺ ratio. Comparisons among levels of (A) % NaCl stress, (B) Stress severity, (C) AM taxa, (D) Host water status, (E) Host type, (F) Woodiness, and (G) Shoot size. p ≤ 0.05 indicates that the moderator level was significantly different than zero. The absent forest plot for “AM lower” in (D) reflects insufficient studies to have included that moderator level in the meta-analysis.

Figure 3

Weighted summary effect sizes (ln R) and 95% bootstrapped confidence intervals (CIs) for influence of NaCl stress on root K⁺/Na⁺ ratio. Comparisons among levels of (A) % NaCl stress, (B) Stress severity, (C) AM taxa, (D) Host water status, (E) Host type, (F) Woodiness, and (G) Shoot size. p ≤ 0.05 indicates that the moderator level was significantly different than zero. Absent forest plots for a particular level of a moderator reflects insufficient studies to have included that level in the meta-analysis.

Figure 4

Weighted summary effect sizes (ln R) and 95% bootstrapped confidence intervals (CIs) for influence of NaCl stress on root proline. Comparisons among levels of (A) Stress severity, (B) AM taxa, (C) Host type, (D) Woodiness, and (E) Shoot size. p ≤ 0.05 indicates that the moderator level was significantly different than zero. Absent forest plots for a particular level of a moderator reflects insufficient studies to have included that level in the meta-analysis.

Figure 5

Natural log of the response ratio of shoot K⁺/Na⁺ as percent root colonization of plants increases (A) and root K⁺/Na⁺ as time of exposure to NaCl increases (B). Dotted lines above and below the predicted slope are the upper and lower 95% confidence intervals.