Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2019;38(5-6):382-400.
doi: 10.1080/07352689.2019.1693716. Epub 2019 Dec 10.

The expanding world of plant J-domain proteins

Amit K Verma  1 , Chetana Tamadaddi  1 , Yogesh Tak  1 , Silviya S Lal  1 , Sierra J Cole  2 , Justin K Hines  2 , Chandan Sahi  1
Affiliations

The expanding world of plant J-domain proteins

Amit K Verma et al. CRC Crit Rev Plant Sci. 2019.

Abstract

Plants maintain cellular proteostasis during different phases of growth and development despite a barrage of biotic and abiotic stressors in an ever-changing environment. This requires a collaborative effort of a cadre of molecular chaperones. Hsp70s and their obligate co-chaperones, J-domain proteins (JDPs), are arguably the most ubiquitous and formidable components of the cellular chaperone network, facilitating numerous and diverse cellular processes and allowing survival under a plethora of stressful conditions. JDPs are also among the most versatile chaperones. Compared to Hsp70s, the number of JDP-encoding genes has proliferated, suggesting the emergence of highly complex Hsp70-JDP networks, particularly in plants. Recent studies indicate that besides the increase in the number of JDP encoding genes; regulatory differences, neo- and sub-functionalization, and inter- and intra-class combinatorial interactions, is rapidly expanding the repertoire of Hsp70-JDP systems. This results in highly robust and functionally diverse chaperone networks in plants. Here, we review the current status of plant JDP research and discuss how the paradigm shift in the field can be exploited toward a better understanding of JDP function and evolution.

Keywords: Evolution; Hsp40; Hsp70; JDP; plants.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.
Tertiary structure of an Hsp70. The surface and secondary structure of E. coli Hsp70, DnaK, is shown in ‘rainbow color scheme’ (Protein Data Bank ID: 2KHO). The nucleotide binding domain (Left, in blue and green) and substrate binding domain (Right, in red) with a lid domain, are connected by a short hydrophobic linker.
Figure 2.
Figure 2.
The Hsp70-JDP chaperone machinery. A native or non-native client binds to Hsp70 directly or delivered via a JDP. Stimulation of Hsp70 ATP hydrolysis by the J-domain of the JDP leads to stable interaction between Hsp70 and substrate, releasing an inorganic phosphate (Pi). The JDP is recycled for subsequent rounds of interaction with substrate and/or Hsp70. Binding of a nucleotide exchange factor (NEF) stimulates release of ADP, allowing ATP rebinding, which induces allosteric changes in the substrate binding domain (SBD) to release the substrate. ATP-bound Hsp70 and NEF are recycled for further binding and release cycles.
Figure 3.
Figure 3.
J-domain structure and J protein classes. (A) A typical J-domain contains four a-helices as labeled (Protein Data Bank ID: 2OCH from dnj-12 of C. elegans). On a loop connecting helix II and III is the conserved signature His, Pro and Asp (HPD) tripeptide motif, crucial for interaction with the NBD of Hsp70. (B) JDPs are classified into three distinct groups as class I, class II, class III. Class I JDPs contain an N terminal J-domain (J) followed by a region rich in glycine and phenylalanine residues (G/F), four CxxCxGxG type zinc-finger motifs, and a C-terminal region (C-term). Class II is same as class I JDPs in their structural organization, except that they lack zinc-finger motifs. Class III JDPs are more diverse and can have a J-domain at any position in the sequence and may or may not have additional domains and motifs. Besides these, class IV JDPs have a cryptic J-like domain, which is structurally similar to a typical J-domain.
Figure 4.
Figure 4.
JDP-gene duplication may result in functional diversification. (A) The ancestral JDP may possess a multitude of functionalities. After gene duplication events, these functions can often be subdivided into different paralogous proteins that are now capable of performing subsets of specific ancestral functions. (B) The ancestral JDP may duplicate and accommodate mutations that lead either an entirely new function or attain a new function while retaining the ancestral function.
Figure 5.
Figure 5.
Emergence of JDPs paralogs. (A) Orthologous JDPs emerging from a common ancestral JDP first get speciated (in species S1, depicted as pink box and S2, depicted as green box), [1]. Following speciation, JDPs may duplicate leading to the formation of multiple isoforms in respective species. The homologous JDP in the same species either in S1 or S2 is in-paralogs. [2] Mostly these in-paralogs have highly conserved function, shown as yellow JDPs or, [3] can have slightly modified functions, indicated as blue and dark blue JDPs. JDPs of S1 are orthologous to JDPs of S2. (B) The ancestral JDP gets duplicated first in a species, S1. This usually results in different functions of paralogous JDPs, even in same species. Here indicated as yellow and blue protein colors [1]. Subsequent speciation may lead to distribution of these JDPs in different species [2, 3]. This can result in the formation of orthologous JDPs in S1 and S2 having similar functions, here shown as yellow protein color in species S1 and S2, or blue color in species S1 and S2. Now these homologous JDPs in a species, either S1 or S2 are out-paralogs.
Figure 6.
Figure 6.
The Hsp70-JDP network in A. thaliana. Specific JDPs along with partner Hsp70s are represented in cartoon form according to their occurrence in different cell organelles viz. chloroplast, endoplasmic reticulum, ribosomes, peroxisomes, clathrin vesicles, mitochondria, and in cytosol. Below JDPs are listed according to their predicted cellular localization. The TAIR locus of Hsp70s along with their other names are written on the left. The standard names of proteins in A. thaliana are mentioned on right. Those proteins whose orthologs are known, are depicted in bold along with name of their respective yeast orthologs. (Information adapted from Table S2, Verma et al., G3, 2017.)
Figure 7.
Figure 7.
Factors determining the complexity of Hsp70-JDP interactions in multicellular eukaryotes like plants. Spatio-temporal expression: Multiple JDPs may work with common Hsp70 at a particular sub-cellular location, tissue or stage. Functional diversification can result from either sub or neo-functionalization among duplicated JDPs. Combinatorial interactions: JDPs of the same or different class may interact to perform diverse functions with Hsp70 partners.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Altschul SF, Madden TL, Schaffer AA, Zhang J, and Zhang Z 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402. doi:10.1093/nar/25.17.3389 - DOI - PMC - PubMed
    1. Aubert D, Chen L, Moon Y-H, Martin D, Castle LA, Yang C-H, and Sung ZR 2001. EMF1, a novel protein involved in the control of shoot architecture and flowering in Arabidopsis. Plant Cell 13: 1865–1876. doi:10.2307/3871324 - DOI - PMC - PubMed
    1. Barghetti A, Sjogren L, Floris M, Paredes EB, Wenkel S, and Brodersen P 2017. Heat-shock protein 40 is the key farnesylation target in meristem size control, abscisic acid signaling, and drought resistance. Genes Dev. 31: 2282–2295. doi:10.1101/gad.301242.117 - DOI - PMC - PubMed
    1. Battisti DS, and Naylor RL 2009. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323: 240–244. doi:10.1126/science.1164363 - DOI - PubMed
    1. Bekh-Ochir D, Shimada S, Yamagami A, Kanda S, Ogawa K, Nakazawa M, Matsui M, Sakuta M, Osada H, Asami T, and Nakano T 2013. A novel mitochondrial DnaJ/Hsp40 family protein BIL2 promotes plant growth and resistance against environmental stress in brassinosteroid signaling. Planta 237: 1509–1525. doi:10.1007/s00425-013-1859-3 - DOI - PMC - PubMed

LinkOut - more resources