Organelle–nucleus cross-talk regulates plant intercellular communication via plasmodesmata

Abstract

We use Arabidopsis thaliana embryogenesis as a model system for studying intercellular transport via plasmodesmata (PD). A forward genetic screen for altered PD transport identified increased size exclusion limit (ise) 1 and ise2 mutants with increased intercellular transport of fluorescent 10-kDa tracers. Both ise1 and ise2 exhibit increased formation of twinned and branched PD. ISE1 encodes a mitochondrial DEAD-box RNA helicase, whereas ISE2 encodes a DEVH-type RNA helicase. Here, we show that ISE2 foci are localized to the chloroplast stroma. Surprisingly, plastid development is defective in both ise1 and ise2 mutant embryos. In an effort to understand how RNA helicases that localize to different organelles have similar impacts on plastid and PD development/function, we performed whole-genome expression analyses. The most significantly affected class of transcripts in both mutants encode products that target to and enable plastid function. These results reinforce the importance of plastid-mitochondria-nucleus cross-talk, add PD as a critical player in the plant cell communication network, and thereby illuminate a previously undescribed signaling pathway dubbed organelle-nucleus-plasmodesmata signaling. Several genes with roles in cell wall synthesis and modification are also differentially expressed in both mutants, providing new targets for investigating PD development and function.

Plasmodesmata formation and cell-to-cell transport are reduced in decreased size exclusion limit 1 during embryogenesis in Arabidopsis

“…Plastid homeostasis is very important to PD structure and function. GAT1 localizes to plastids (26), and ise1 and ise2 both dramatically affect the expression of more than 300 nuclear genes essential for chloroplast function (30). Finally, a mutant of corn, sucrose export defective 1, with decreased PD mediated transport from the phloem encodes a protein that localizes to chloroplasts (32).…”

“…All five of these mutants produce severe phenotypes during embryo or seedling development; however, except GSL8 none encodes proteins that localize to PD. ISE1 encodes a mitochondrial DEAD-box RNA helicase (22), ISE2 encodes a chloroplast DEVH-type RNA helicase (23,30), GAT1 encodes a chloroplast thioredoxin (26), and DSE1 encodes a WDR protein that localizes to the nucleus and cytoplasm. Only, GSL8 encodes a putative glucan synthase, that may localize close to PD, as it is involved in callose deposition in cell walls at the cell plate (31).…”

Influence of plastids on light signalling and development

“…Blocking chloroplast biogenesis with a norflurazon treatment appeared to affect leaf size in part by inhibiting the transition from cell-proliferation-based morphogenesis to cell-expansion-based morphogenesis [38]. Deficiencies in mitochondrial and chloroplastic RNA helicases affected nuclear gene expression and promoted the formation and function of plasmodesmata [70].…”

Chloroplasts extend stromules independently and in response to internal redox signals

“…In recent years, forward genetic screens have led to the discoveries that chloroplasts are critical regulators of leaf shape, cell-cell signaling through plasmodesmata, pathogen defense, and even alternative splicing in the nucleus (1)(2)(3)(4)(5)(6)(7)(8); however, in almost all of these pathways, the signaling route between the chloroplast and the nucleus is unknown. This is a pressing question for plant biology and cell biology in general: how do organelles communicate with the nucleus to coordinate genetic programs and cellular function?…”