Nitric Oxide Plays a Role in Stem Cell Niche Homeostasis through Its Interaction with Auxin

Abstract

Nitric oxide (NO) is a unique reactive nitrogen molecule with an array of signaling functions that modulates plant developmental processes and stress responses. To explore the mechanisms by which NO modulates root development, we used a pharmacological approach and NO-deficient mutants to unravel the role of NO in establishing auxin distribution patterns necessary for stem cell niche homeostasis. Using the NO synthase inhibitor and Arabidopsis (Arabidopsis thaliana) NO biosynthesis mutants (nitric oxide-associated1 [noa1], nitrate reductase1 [nia1] and nia2, and nia1 nia2 noa1), we show that depletion of NO in noa1 reduces primary root elongation and increases flavonol accumulation consistent with elevated reactive oxygen species levels. The elevated flavonols are required for the growth effect, because the transparent testa4 mutation reverses the noa1 mutant root elongation phenotype. In addition, noa1 and nia1 nia2 noa1 NO-deficient mutant roots display small root meristems with abnormal divisions. Concomitantly, auxin biosynthesis, transport, and signaling are perturbed. We further show that NO accumulates in cortex/endodermis stem cells and their precursor cells. In endodermal and cortical cells, the noa1 mutant acts synergistically to the effect of the wuschel-related homeobox5 mutation on the proximal meristem, suggesting that NO could play an important role in regulating stem cell decisions, which has been reported in animals.Root growth enables plants to explore their substrate and extract nutrients and water from larger areas and greater depths while also providing anchorage to the substrate. To properly regulate primary root elongation, multiple intrinsic and extrinsic signals must be integrated. Plant hormones are important long-distance signals, and auxin in particular regulates many aspects of root development. Auxin regulates primary root growth in three important ways: by positioning the stem cell niche, affecting divisions in a transit-amplifying zone known as the meristem, and increasing cell volume in the elongation zone (for review, see Bennett and Scheres, 2010). These processes are dependent on the establishment of auxin gradients. Models generated on the basis of available information predict a maximum auxin concentration in the quiescent center (QC) and a steep auxin gradient in the proximal meristem, which decreases with distance to the QC (Grieneisen et al., 2007;Kramer et al., 2008;Laskowski et al., 2008).Interestingly, reactive oxygen species (ROS) and reactive nitrogen species (RNS) have been found to play an important role in the response to intrinsic and extrinsic growth-modulating signals. Research over the last decades has shown several crucial roles of nitric oxide (NO; an RNS) during plant development. NO is involved in the promotion of seed germination and alleviation of seed dormancy, the shaping of root architecture, the repression of floral transition, and the regulation of mitochondrial respiratory complexes, stomatal closure, fruit maturation, senescence, and iron metaboli...

The Nitrification Inhibitor Methyl 3-(4-Hydroxyphenyl)Propionate Modulates Root Development by Interfering with Auxin Signaling via the NO/ROS Pathway

“…Previous studies revealed that disrupting NO production reduced DR5:GUS expression in roots (Sanz et al, 2014). NO also affected auxin signaling by promoting the degradation of IAA17 (Terrile et al, 2012).…”

“…The NO biosynthesisrelated triple mutant nitrate reductase1 (nia1)/nia2/noa1 exhibits reduced NO levels and small root meristems with abnormal divisions. Further investigation indicated that the abnormal phenotypes of this NO mutant are related to perturbations in auxin biosynthesis, transport, and signaling (Sanz et al, 2014).…”

Nitric Oxide: A Multitasked Signaling Gas in Plants

“…of stem-cell decisions through its interaction with auxin (Sanz et al, 2014). During Arabidopsis cell growth in the root apical meristem, PIN1-dependent acropetal auxin transport was reduced when high levels of NO were applied, which has been interpreted as a result of the inhibition of polar auxin transport, and may imply that NO acts downstream of auxin (Ferná ndez-Marcos et al, 2011.…”

“…NO generation has also been shown to interfere with various auxindependent responses such as root development Correa-Aragunde et al, 2004) and auxin-mediated gravitropism (Hu et al, 2005). Recently NO was also postulated to interact with auxins to regulate the homeostasis of the stem-cell niche (Sanz et al, 2014). NO also appears to influence root development through the initiation of cell-cycle genes and patterns of cellulose synthesis (Correa-Aragunde et al, 2006.…”

Serotonin modulates Arabidopsis root growth via changes in reactive oxygen species and jasmonic acid–ethylene signaling

“…Taken together, our results suggest that the serotonin-induced root growth inhibition in WT seedlings is likely because of a ROS imbalance at the primary root tip likely affecting cell division, elongation or both of these processes. In this regard, reduced primary root growth in plants that overaccumulate ROS in root tips in response to different stimuli have been recently reported, such as reduced primary root growth in NO-deficient mutants such as in the triple mutant nia1 nia2 noa1, which correlate with an enhanced ROS accumulation and suppression of auxin activity (Sanz et al 2014). ROS production in primary roots in response to boron deficiency was associated with a rapid inhibition of root cell elongation mediated by a signaling pathway triggered by an impaired cell wall integrity caused by the boron deficiency in a process that also involve the participation of Et and auxin (Camacho-Cristóbal et al 2015).…”