Overexpression of the JAZ factors with mutated jas domains causes pleiotropic defects in rice spikelet development

Abstract

In a determinate meristem, such as a floral meristem, a genetically determined number of organs are produced before the meristem is terminated. In rice, iterative formation of organs during flower development with defects in meristem determinacy, classically called 'proliferation', is caused by several mutations and observed in dependence on environmental conditions. Here we report that overexpression of several JAZ proteins, key factors in jasmonate signaling, with mutations in the Jas domains causes an increase in the numbers of organs in florets, aberrant patterns of organ formation and repetitious organ production in spikelets. Our results imply that JAZ factors modulate mechanisms that regulate meristem functions during spikelet development.Meristems provide cells that differentiate and produce organs to sustain plant growth. In indeterminate meristems, such as vegetative and inflorescence meristems, meristematic activity is maintained by continuous cell proliferation balanced with cell differentiation. By contrast in determinate meristems, such as floral meristems, meristematic activity ceases after initiation of a certain number of organs. In general, floral meristem determinacy is regulated genetically. In Arabidopsis, for example, AGA-MOUS has a role in repression of WUSCHEL that is required for maintenance of stem cells in the meristem during flower development (for a review see ref. 1). Strong agamous mutant alleles develop a set of floral organs (sepals-petals-petals) repeatedly, instead of carpel formation, reflecting prolonged maintenance of an active meristem at the center of the flower.1 In rice, flower development occurs in a spikelet, a special inflorescence unit, which produces 2 rudimentary glumes and 2 sterile lemmas and a floret that comprises floral organs (pistil, stamen and lodicule) and outer organs (palea and lemma) (for reviews see refs. 2-3). Determinacy of the floral meristem in rice is controlled by OsMADS58, 4 whereas determinacy of the spikelet meristem and transition of the spikelet meristem to the floral meristem is regulated by OsMADS1/LEAFY HULL STERILE1 (LHS1).3,5 Indeterminate development of flowers consisting of lodicules, stamens and caperl-like organ, but not palea and lemma, was caused by RNA siliencing of OsMADS58. 4 In lhs1 mutants, an additional flower generation in a floret and repetitious formation of leaf-like paleae and lemmas within a spikelet is often observed. 2,5In rice, various types of abnormal spikelet development are induced by cold weather. These include an increase in the number of spikelet organs and formation of multiple-floret spikelets. 6 Moreover, findings of 'proliferated propagule spikelet' formation has been reported in a field survey of cold damages and is characterized by development of foliaceous glumes and leaves in a spikelet, 6 resembling the phenotype observed in lhs1 as described above. Takeoka and Shimizu (1973) 7 reported similar defects in a rice mutant where repetitious formation of vegetative organs ('leafy-shoot-type proliferation'...

A Genome-Wide Analysis Reveals Stress and Hormone Responsive Patterns of TIFY Family Genes in Brassica rapa

“…To gain insight into the potential developmental roles of B. rapa TIFY genes, we selected the JAZ genes for further analysis, as these genes make up the largest portion of the TIFY genes and have been reported to be involved in growth regulatory functions related to organ, especially flower development (Chini et al, 2007 ; Chung et al, 2009 ; Song et al, 2011 ; Hori et al, 2014 ; Yuan and Zhang, 2015 ). First, we conducted semi-quantitative RT-PCR analysis using specific primers with equal amounts of cDNA templates prepared from the mRNA of roots, stems, leaves, and flower buds of healthy, unstressed B. rapa plants to study the organ-specific expression patterns of JAZ genes.…”

The OsJAZ1 degron modulates jasmonate signaling sensitivity during rice development

“…In addition, overexpression of mutated OsJAZ proteins (mJAZ with R 6 R 7 or R 6 K 7 substitution by A 6 A 7 ) also affected spikelet meristem identity and determinacy (Hori et al, 2014), which indicates that OsJAZ degrons play similar roles to those of Arabidopsis JAZ degrons in shaping OsJAZ-OsCOI1b co-receptor interactions to implement JA-steered responses. But, the abnormal spikelet development was more severe in the overexpression of mJAZ lines than that seen in the osjaz1/eg2-1D mutant (Hori et al, 2014), which suggests that the mJAZ degron (XXPXAAA; X is any amino acid) might be more stable or insensitive to OsCOI1-dependent protein degradation than that of the EG2-1D degron (DLPIGRR). To clarify this finding, we investigated how changes to the OsJAZ degron in OsJAZ1 affected its ability to interact with COI and MYC proteins, and how these changes impacted rice development.…”

“…Upon JA binding, the JAZ proteins are destroyed by SKP1-CUL1-F-box protein (SCF) COI1 -mediated 26S proteasome, which releases JAZ-interacting TFs, such as MYC and MYB family members, and other TFs, to drive gene expression and thus change growth responses (Chico et al, 2008;Howe et al, 2018;Pauwels and Goossens, 2011;Wager and Browse, 2012). Hence, changes to JAZ protein stability and/or protein variants affect plant development (Cai et al, 2014;Chini et al, 2007;Chung et al, 2010;Chung and Howe, 2009;Gimenez-Ibanez et al, 2017;Hori et al, 2014;Hu et al, 2016;Huang et al, 2017;Oh et al, 2013;Song et al, 2011;Thines et al, 2007;Thireault et al, 2015;Yang et al, 2012;Yu et al, 2016;Zhai et al, 2015).…”

“…In the osjaz1/extra glumes (eg) 2-1D dominant mutant, a substitution of Ala 5 (A 5 ) by Gly 5 (G 5 ) was identified in the OsJAZ1 degron (DLPIA 5 RR changed to DLPIG 5 RR), which blocked interaction between EG2-1D and OsCOI1b and, in turn, repressed E class MADS-box TF genes, such as OsMADS1, which resulted in the delayed transition of spikelet meristem to floral meristem (Cai et al, 2014). In addition, overexpression of mutated OsJAZ proteins (mJAZ with R 6 R 7 or R 6 K 7 substitution by A 6 A 7 ) also affected spikelet meristem identity and determinacy (Hori et al, 2014), which indicates that OsJAZ degrons play similar roles to those of Arabidopsis JAZ degrons in shaping OsJAZ-OsCOI1b co-receptor interactions to implement JA-steered responses. But, the abnormal spikelet development was more severe in the overexpression of mJAZ lines than that seen in the osjaz1/eg2-1D mutant (Hori et al, 2014), which suggests that the mJAZ degron (XXPXAAA; X is any amino acid) might be more stable or insensitive to OsCOI1-dependent protein degradation than that of the EG2-1D degron (DLPIGRR).…”

Genome-wide characterization of JASMONATE-ZIM DOMAIN transcription repressors in wheat (Triticum aestivum L.)

“…Overexpression of modified AtJAZ1 (lack of Jas domain) is able to enhance host resistance to Spodoptera exigua in Arabidopsis [ 35 ]. Overexpressing the modified OsJAZs can cause the malformation of flower organ in rice [ 36 ]. According to the above researches, JAZ genes have important effects on regulating the adaptability to biotic and abiotic stresses and maintaining the normal development in plants.…”