Review
The PEAPOD Pathway and Its Potential To Improve Crop Yield

https://doi.org/10.1016/j.tplants.2020.10.012Get rights and content

Highlights

  • The TIFY proteins PEAPOD (PPD)1 and PPD2 recruit KINASE-INDUCIBLE DOMAIN INTERACTING PROTEIN (KIX)8, KIX9, and NOVEL INTERACTOR OF JAZ to form repressor complexes that participate in the transcriptional machinery based on their binding partners.

  • STERILE APETALA (SAP)-mediated proteasome-dependent degradation regulates the abundance of PPD and KIX proteins.

  • The PPD/KIX/SAP module is widely conserved among higher plant species (excluding monocot grasses) and regulates leaf, flower, fruit, and seed development in several crop species of agricultural importance.

  • Emerging evidence suggests that the PPD pathway has a wider role in controlling cell proliferation and developmental plasticity in a tissue-, developmental state-, and/or environmental context-dependent manner than anticipated originally.

A key strategy to increase plant productivity is to improve intrinsic organ growth. Some of the regulatory networks underlying organ growth and development, as well as the interconnections between these networks, are highly conserved. An example of such a growth-regulatory module with a highly conserved role in final organ size and shape determination in eudicot species is the PEAPOD (PPD)/KINASE-INDUCIBLE DOMAIN INTERACTING (KIX)/STERILE APETALA (SAP) module. We review the proteins constituting the PPD pathway and their roles in different plant developmental processes, and explore options for future research. We also speculate on strategies to exploit knowledge about the PPD pathway for targeted yield improvement to engineer crop traits of agronomic interest, such as leaf, fruit, and seed size.

Section snippets

JAZ and PPD Proteins: So Similar, Yet So Different

Various regulators of organ size, shape, and differentiation, their targets, interacting proteins, and the interconnections among them have been described [1., 2., 3., 4., 5., 6.]. One such pathway that has highly conserved functions in the development of distinct plant organs in various eudicot species is the PEAPOD (PPD) pathway. PPD1 and PPD2 are transcriptional regulators that, together with the JASMONATE ZIM-DOMAIN (JAZ) proteins and TIFY DOMAIN PROTEIN 8 (TIFY8), constitute the

Leaf Development

In arabidopsis, PPD1/2 and KIX8/9 limit asymmetric divisions of meristemoids – triangular stem-cell like cells that can divide reiteratively before differentiating into stomata [45,48., 49., 50., 51., 52.]. Upon downregulation of PPD or KIX or upregulation of SAP, arabidopsis plants display propeller-like rosettes with enlarged dome-shaped leaves and increased meristemoid asymmetric cell divisions (Figure 2A) [45., 46., 47.]. In addition to limiting meristemoid proliferation in leaves [45],

PPD1/PPD2 and KIX8/KIX9 Control Organ Growth in a Partially Redundant Manner

In arabidopsis, genomic PPD1 or PPD2 transgenes can rescue the Δppd [51] and ami-ppd [43] mutant leaf size and shape phenotypes. In addition, overexpression of PPD1 or PPD2 results in the production of small seeds, whereas seed area, seed weight, and leaf area are significantly increased in ppd1 ppd2-cr and ppd1-cr ppd2 double mutants compared to the respective single mutants (Table 1) [42,83]. In agreement, PPD1 and PPD2 are expressed in an overlapping manner in arabidopsis, including young

Why Are PPD/KIX/SAP Orthologs Absent in Poaceae?

Although they are absent in non-photosynthetic eukaryotes and green algae, several TIFY protein family members have orthologs in monocot and eudicot species [7,8,41,121., 122., 123., 124., 125., 126., 127.]. Interestingly, however, although they are highly conserved in both sequence and function across rosid and asterid species that constitute most of the core eudicots [46,47,60., 61., 62.,64,69], PPD/KIX/SAP orthologs appear to be absent in Poaceae (grasses) [43,45,46]. The phylogenetic

Targeting the PPD Pathway to Improve Specific Plant Agronomic Traits

The significant increases in shoot, fruit, and seed biomass in multiple eudicots upon downregulation of PPD or KIX [42,45,51,60,62., 63., 64.,69] or upregulation of SAP genes [46,47,61,67,68] imply that the PPD pathway may hold great potential from a biotechnological point of view (Table 1 and Figure 3). Increased fruit size, for instance, as observed in Slkix8-kix9 tomato [69], ele1 and bio pea [63], and SAP-overexpressing cucumber lines [67], was among the main selection criteria for nearly

Concluding Remarks and Future Perspectives

An increasing number of studies highlight a conserved role for the PPD pathway in regulating organ growth in various eudicot species, predominantly by restricting cell proliferation, and reveal interconnections with other growth-regulatory modules, although the evidence is often preliminary and lacks strong evidence. Nonetheless, these findings indicate that targeting the PPD pathway may hold great potential for targeted yield improvement of crops of high agricultural and economic value. The

Acknowledgments

The authors would like to thank Annick Bleys for proofreading and submitting the manuscript. This work was supported by Ghent University (BOF-Methusalem projects BOFMET2015000201 and B/09140/02) and by the Research Foundation Flanders (FWO research project 3G038719).

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