Bacillus amyloliquefaciens SAY09 Increases Cadmium Resistance in Plants by Activation of Auxin-Mediated Signaling Pathways

Abstract

Without physical contact with plants, certain plant growth-promoting rhizobacteria (PGPR) can release volatile organic compounds (VOCs) to regulate nutrient acquisition and induce systemic immunity in plants. However, whether the PGPR-emitted VOCs can induce cadmium (Cd) tolerance of plants and the underlying mechanisms remain elusive. In this study, we probed the effects of Bacillus amyloliquefaciens (strain SAY09)-emitted VOCs on the growth of Arabidopsis plants under Cd stress. SAY09 exposure alleviates Cd toxicity in plants with increased auxin biosynthesis. RNA-Seq analyses revealed that SAY09 exposure provoked iron (Fe) uptake- and cell wall-associated pathways in the Cd-treated plants. However, SAY09 exposure failed to increase Cd resistance of plants after treatment with 1-naphthylphthalamic acid (NPA) or 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (c-PTIO). Under Cd stress, SAY09 exposure markedly promoted Fe absorption in plants with the increased hemicellulose 1 (HC1) content and Cd deposition in root cell wall, whereas these effects were almost abrogated by treatment with NPA or c-PTIO. Moreover, exogenous NPA remarkably repressed the accumulation of nitric oxide (NO) in the SAY09-exposed roots under Cd stress. Taken together, the findings indicated that NO acted as downstream signals of SAY09-induced auxin to regulate Fe acquisition and augment Cd fixation in roots, thereby ameliorating Cd toxicity.

Arabidopsis Transcription Factor MYB102 Increases Plant Susceptibility to Aphids by Substantial Activation of Ethylene Biosynthesis

“…Then, cDNA samples were used as the templates of qRT-PCR to examine transcript abundance of target genes including MYB102, FMO1, SAUR20, CYP708A1, MIOX2, PEN4, BGLU31, THI2.1, TPS20, KCS15 , and TPS3. qRT-PCR reaction was carried out using the TBGreen™Premix ExTaq™II (Takara, Dalian, China) in an Applied Biosystems (ABI) 7500 PCR machine (Applied Biosystems, Carlsbad, CA, USA) according to the methods reported by Zhou et al [ 62 ]. To normalize gene expression levels, the ACTIN2 gene was selected as an internal control.…”

“…Arabidopsis plants carrying pMYB102:GUS were stained by histochemical analyses according to the methods described by Zhou et al [ 62 ]. Plant samples were incubated with the staining solution containing 0.1 M sodium phosphate buffer (pH 7.2), 0.1% ( v / v ) Triton X-100, 2 mM potassium ferrocyanide and potassium ferricyanide, 2 mM 5-bromo-4-chloro-3-indolylglucuronide (X-Gluc) for 16 h at 37 °C.…”

Induced Systemic Resistance (ISR) and Fe Deficiency Responses in Dicot Plants

“…Besides ET, other hormones and signaling molecules, such as auxin, GSH and NO have also been involved in both ISR and Fe deficiency responses ( Ribaudo et al, 2006 ; Graziano and Lamattina, 2007 ; Bacaicoa et al, 2009 , 2011 ; Chen et al, 2010 ; García et al, 2010 , 2011 , 2018 ; Acharya et al, 2011 ; Romera et al, 2011 , 2017 ; Jin et al, 2014 ; Contreras-Cornejo et al, 2015 ; Shanmugam et al, 2015 ; Zamioudis et al, 2015 ; Garnica-Vergara et al, 2016 ; Poupin et al, 2016 ; Zhou et al, 2016a , 2017 , 2018 ; Wang J. et al, 2017 ; Gullner et al, 2018 ; Kailasam et al, 2018 ; Sharifi and Ryu, 2018 ; Stringlis et al, 2018a ; Sumayo et al, 2018 ; Tyagi et al, 2018 ). All of them increase in roots under Fe deficiency and frequently upon colonization of roots by ISR-eliciting microbes ( Romera et al, 1999 ; Ribaudo et al, 2006 ; Graziano and Lamattina, 2007 ; Bacaicoa et al, 2009 , 2011 ; Chen et al, 2010 ; Contreras-Cornejo et al, 2015 ; Shanmugam et al, 2015 ; Zamioudis et al, 2015 ; Zhou et al, 2016a , 2017 ; Wang J. et al, 2017 ; Kailasam et al, 2018 ). Some microbial elicitors, like VOCs or LPS, can affect ET, auxin or NO production and/or signaling, and in this way upregulate Fe-related genes ( Zeidler et al, 2004 ; Zhang et al, 2007 , 2009 ; Kwon et al, 2010 ; Liu and Zhang, 2015 ; Zamioudis et al, 2015 ; Garnica-Vergara et al, 2016 ; Zhou et al, 2017 ; Wang J. et al, 2017 ; Sharifi and Ryu, 2018 ; Tyagi et al, 2018 ).…”

“…All of them increase in roots under Fe deficiency and frequently upon colonization of roots by ISR-eliciting microbes ( Romera et al, 1999 ; Ribaudo et al, 2006 ; Graziano and Lamattina, 2007 ; Bacaicoa et al, 2009 , 2011 ; Chen et al, 2010 ; Contreras-Cornejo et al, 2015 ; Shanmugam et al, 2015 ; Zamioudis et al, 2015 ; Zhou et al, 2016a , 2017 ; Wang J. et al, 2017 ; Kailasam et al, 2018 ). Some microbial elicitors, like VOCs or LPS, can affect ET, auxin or NO production and/or signaling, and in this way upregulate Fe-related genes ( Zeidler et al, 2004 ; Zhang et al, 2007 , 2009 ; Kwon et al, 2010 ; Liu and Zhang, 2015 ; Zamioudis et al, 2015 ; Garnica-Vergara et al, 2016 ; Zhou et al, 2017 ; Wang J. et al, 2017 ; Sharifi and Ryu, 2018 ; Tyagi et al, 2018 ). As examples, VOCs from Bacillus subtilis GB03 upregulated the expression of several ET biosynthesis genes ( Kwon et al, 2010 ) and VOCs from P. simiae WCS417 or Bacillus amyloliquefaciens BF06 caused NO accumulation in Arabidopsis roots and upregulated several Fe-related genes ( Zamioudis et al, 2015 ; Wang J. et al, 2017 ).…”

Cadmium-tolerant endophytic Pseudomonas rhodesiae strains isolated from Typha latifolia modify the root architecture of Arabidopsis thaliana Col-0 in presence and absence of Cd

“…t h a l i a n a s e e d l i n g s i n o c u l a t e d w i t h Bacill us amyloliquefaciens SAY09. This bacterium synthesizes IAA and volatile organic compounds, which activate auxinmediated signaling pathways to increase Cd tolerance in A. thaliana seedlings [60].…”