Low pH-induced cell wall disturbances in Arabidopsis thaliana roots lead to a pattern-specific programmed cell death in the different root zones and arrested elongation in late elongation zone

Jonathas Pereira Graças (1, 2, 3) , Mariana Belloti (4) , Joni Esrom Lima (1) , Lázaro Eustáquio Pereira Peres (2) , Vincent Burlat (5) , Elisabeth Jamet (5) , Victor Alexandre Vitorello (4)

1 UFMG - Universidade Federal de Minas Gerais = Federal University of Minas Gerais [Belo Horizonte, Brazil]
2 ESALQ - Escola Superior de Agricultura "Luiz de Queiroz"
3 LRSV - Laboratoire de Recherche en Sciences Végétales
4 CENA - Centro de Energia Nuclear na Agricultura
5 Dynamique et Evolution des Parois cellulaires végétales

Low pH stress (pH < 5.5) triggers sensitivity responses in roots such as cell death (CD) or arrest in elongation which are detrimental to the development of many plant species. The involvement of the cell wall (CW) with these sensitive responses and their spatiotemporal dynamics in the distinct root zones remains poorly understood. The spatio-temporal analysis of primary roots of Arabidopsis thaliana upon low pH (pH 4.6) revealed that the CD repeatedly started in cells of the transition zone (TZ). Then, CD dynamically moved downward to the meristematic zone (MZ) and upward to the early elongation zone (EZ). The dead cells exhibited coordinated in situ DNA fragmentation, highlighted by the deformity in the nuclei of dead cells and positive reaction for Terminal Deoxynucleotidyl Transferase-mediated dUTP Nick-End Labeling (TUNEL). This DNA fragmentation strongly suggests that the low pH-driven CD occurred through a programmed cell death (PCD) pathway. In addition, a decreased CW stiffness in TZ epidermal cells before the onset of CD suggests that low pH first triggers cell wall disturbances (CWDs) in these root cells. Disruption in CW integrity caused by incorrect cellulose deposition in cobra (cob-1) mutant enhanced CD in TZ and early EZ. Supporting this notion, an increase in calcium concentration upon low pH alleviated the CD in roots, probably due to its role in stabilization of the pectin crosslinking in CWs and likely counteracting the low pH-induced CWDs. Moreover, the CD was significantly decreased when roots were exposed to low pH under reduced CW tension, however, a sudden increase in turgor pressure and CW tension (hypoosmotic treatment) combined with low pH accelerated CD in TZ and early EZ. The CD was not observed in the wild type late EZ trichoblasts upon low pH but rather an orchestrated arrest in elongation. An increase in calcium concentration inhibited this elongation arrest upon low pH, suggesting that the onset of this response also required CWDs. Altogether, these results indicate that low pH-induced CWDs triggered sensitive responses within defined root zones. The low pH-activated PCD and an orchestrated elongation arrest occurring in different root zones suggest the occurrence of yet to be identified signaling cascades.

Mots clés: Acidic stress; Cell mortality; Cell wall integrity; Cell wall stiffness; Root zone

Domaines: Biologie végétale

Jonathas Pereira Graças, Mariana Belloti, Joni Esrom Lima, Lázaro Eustáquio Pereira Peres, Vincent Burlat, et al.. Low pH-induced cell wall disturbances in Arabidopsis thaliana roots lead to a pattern-specific programmed cell death in the different root zones and arrested elongation in late elongation zone. Environmental and Experimental Botany, 2021, 190, pp.104596. ⟨10.1016/j.envexpbot.2021.104596⟩. ⟨hal-03437134⟩