Indole-3-Butyric Acid Induces Ectopic Formation of Metaxylem in the Hypocotyl of Arabidopsis thaliana without Conversion into Indole-3-Acetic Acid and with a Positive Interaction with Ethylene

Abstract

The role of the auxins indole-3-acetic acid (IAA) and indole-3-butyric acid (IBA) and of the auxin-interacting phytohormone ethylene, on the ectopic formation of primary xylem (xylogenesis in planta) is still little known. In particular, auxin/ethylene-target tissue(s), modality of the xylary process (trans-differentiation vs. de novo formation), and the kind of ectopic elements formed (metaxylem vs. protoxylem) are currently unknown. It is also unclear whether IBA may act on the process independently of conversion into IAA. To investigate these topics, histological analyses were carried out in the hypocotyls of Arabidopsis wild type seedlings and ech2ibr10 and ein3eil1 mutants, which are blocked in IBA-to-IAA conversion and ethylene signalling, respectively. The seedlings were grown under darkness with either IAA or IBA, combined or not with the ethylene precursor 1-aminocyclopropane-1-carboxylic acid. Adventitious root formation was also investigated because this process may compete with xylogenesis. Our results show that ectopic formation of protoxylem and metaxylem occurred as an indirect process starting from the pericycle periclinal derivatives of the hypocotyl basal part. IAA favoured protoxylem formation, whereas IBA induced ectopic metaxylem with ethylene cooperation through the EIN3EIL1 network. Ectopic metaxylem differentiation occurred independently of IBA-to-IAA conversion as mediated by ECH2 and IBR10, and in the place of IBA-induced adventitious root formation.

Cellular dynamics during maturation‐related decline of adventitious root formation in forest tree species

“…The inductive stimulus and auxin accumulation in the progenitor cells also appear crucial for the induction of xylem formation both in planta and in vitro (Sundberg et al , De Almeida et al , Della Rovere et al , Fattorini et al ). Tracheid nests in association with small local areas of meristematic cells within the callus from peach palm explants (De Almeida et al ), and tracheary‐like cells found during the initial divisions leading to the direct organization of an adventitious root meristem in hypocotyls from P. taeda and P. radiata (Díaz‐Sala, unpublished) are the first visible signs of differentiation.…”

“…long generation time, lack of mutants, difficulties in transformation and regeneration procedures) hamper the functional elucidation of cellular and molecular mechanisms underlying the capacity to form adventitious roots in woody species. Model species, such as Arabidopsis thaliana (Arabidopsis), are used to overcome this limitation and to address functional studies of adventitious rooting and age‐related decline of adventitious root formation (Díaz‐Sala et al , Della Rovere et al , Bellini et al , Abu‐Abied et al , , Fattorini et al ). In Arabidopsis, the hypocotyl pericycle cells may be switched toward either adventitious root formation or xylogenesis by the same inductive treatment, depending on the induction of a different orientation of the cell division planes; anticlinal for the induction of adventitious root formation or periclinal for the induction of xylogenesis.…”

“…The adventitious root response is triggered in the presence of exogenous auxin plus cytokinin. Anticlinal cell divisions are induced in the pericycle derivatives, leading to adventitious root primordia along the length of the hypocotyl, as opposed to the induction of cell divisions in pericycle cells at the base of the hypocotyl that follow periclinal division planes, further differentiating into ectopic metaxylem (Della Rovere et al , , Fattorini et al ). The auxin influx carrier AUX1, and the transcription factors SHORT‐ROOT (SHR) and SCARECROW (SCR) are involved in the balance and switching between xylem development and adventitious root formation (Della Rovere et al ).…”

“…The auxin influx carrier AUX1, and the transcription factors SHORT‐ROOT (SHR) and SCARECROW (SCR) are involved in the balance and switching between xylem development and adventitious root formation (Della Rovere et al ). Auxin and ethylene are also determinants for the equilibrium between adventitious root formation and xylem development in the adventitious rooting cells of the hypocotyl pericycle in Arabidopsis (Fattorini et al ). Histological and histochemical analyses have shown that pre‐procambial cells provide niches for multipotent cells for vascular differentiation, organogenesis, or somatic embryogenesis, depending on the positioning of the competent cells and their interaction with neighboring cells in peach palm explants.…”

EIN2 and COI1 control the antagonism between ethylene and jasmonate in adventitious rooting of Arabidopsis thaliana thin cell layers

“…The same as AR-formation, xylogenesis is an auxin-induced program, and may be a concomitant/ alternative program to AR-formation (Ricci et al 2016, and references therein). In Arabidopsis, the competitive realization of xylogenesis is known to reduce AR-formation in seedlings and TCLs (Fattorini et al 2017a(Fattorini et al , 2018. In WT TCLs treated with IBA + ACC a conspicuous production of xylary cells was observed (Fig.…”