Continuous expression of genes for xylem cysteine peptidases in long-lived ray parenchyma cells in <i>Populus</i>

Abstract

XYLEM CYSTEINE PEPTIDASE 1 (XCP1) and XCP2 are key autolytic enzymes in programmed cell death of short-lived tracheary elements in plants. However, the patterns of expression of XCP genes remain to be clarified in long-lived ray parenchyma cells, which survive for several years after the completion of secondary wall formation. We isolated full-length cDNAs that encoded three XCPs (PsgXCP1, PsgXCP2A and PsgXCP2B) of Populus. The deduced amino acid sequences of the XCPs revealed three conserved catalytic residues, namely, cysteine (Cys), histidine (His) and asparagine (Asn), indicating that PsgXCP1, PsgXCP2A and PsgXCP2B might function as papain-like cysteine proteases. Ray parenchyma cells in hybrid poplar remained alive for several years, with continuous expression of XCP genes even after obvious secondary wall thickenings. Levels of expression of XCP genes were lower in the innermost annual ring of sapwood than in one and/or two outer annual rings from beyond the innermost sapwood. This result implies that autolysis of ray parenchyma cells might not be fully explained by dramatically enhanced expression of XCP genes just before their programmed death. In addition, the expression of PtaSND1-A1, PtaVND6-A1 and PtaMYB003 genes was detected in all annual ring in sapwood. Our observations suggest that the expression of genes associated with xylem differentiation such as secondary wall formation and cell death continues for several years in long-lived ray parenchyma cells before their death.

Differential Gene Profiling of the Heartwood Formation Process in Taiwania cryptomerioides Hayata Xylem Tissues

“…Two closely related cysteine proteases, XCP1 (xylem cysteine protease 1) and XCP2, are considered key autolytic enzymes produced for the PCD of TEs [43], and these two genes were highly expressed before the cell death of vessel or fiber cells [48,49]. However, similar to the expression pattern of our XBCP gene, the expressions of these two XCP genes in the ray parenchyma cells of Populus showed decreases from outer SW toward inner SW, where the ray parenchyma cells gradually die [50]. This indicates that the cell death mechanism of ray parenchyma cells during the HW formation process might not fully resemble that in TE differentiation.…”

Plant life needs cell death, but does plant cell death need Cys proteases?

“…Multiple components of TE differentiation and PCD have been identified using an in vitro system that induces differentiation of mesophyll cells of Zinnia elegans into TEs upon hormone treatment. The PCD process appears to be initiated through the activity of at least two NAC transcription factors: Vascular‐related NAC Domain 6 (VND6) and VND7 in Arabidopsis thaliana (Arabidopsis) and poplar . Loss of tonoplast integrity and the concomitant rupture of the vacuole are considered to be the actual moment of cell death during TE differentiation .…”

Plant proteases during developmental programmed cell death

“…Although accumulation of XCPs seems to be part of xylem Downloaded from https://academic.oup.com/jxb/advance-article-abstract/doi/10.1093/jxb/erz072/5358628 by Ghent University user on 06 March 2019 A c c e p t e d M a n u s c r i p t 9 differentiation, their activation seems to be confined to precise developmental stages. Despite the transcriptional accumulation of PsgXCP1, PsgXCP2A, and PsgXCP2B in poplar, ray parenchyma cells (radially arranged cells in woody tissues) remained alive for extended periods of time, even after secondary cell wall deposition (Nakaba et al, 2015). Despite the fact that ray parenchyma cells might follow differentiation programs distinct from TEs, this finding suggests that XCP proteases have to be post-transcriptionally activated in order to affect post-mortem clearance.…”

“…VND6 (VASCULAR-RELATED NAC-DOMAIN 6) and VND7 are two central NAC transcription factors implicated in xylem differentiation in Arabidopsis and poplar (Populus spec.) (Nakaba et al, 2015;Ohashi-Ito et al, 2010;Yamaguchi et al, 2010). Closely related NAC transcription factors have been implicated in xylem development of other species, including gymnosperms and non-vascular plants (Duval et al, 2014;Laubscher et al, 2018;Xu et al, 2014), suggesting a high degree of evolutionary conservation of xylem differentiation.…”