SAG12, a Major Cysteine Protease Involved in Nitrogen Allocation during Senescence for Seed Production in Arabidopsis thaliana

James, Maxence; Poret, Marine; Masclaux-Daubresse, Céline; Marmagne, Anne; Coquet, Laurent; Jouenne, Thierry; Chan, Philippe; Trouverie, Jacques; Étienne, Philippe

doi:10.1093/pcp/pcy125

Cited by 75 publications

(69 citation statements)

References 51 publications

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“…S7). The lack of phenotypic differences between the pp2a-b9g and pp2a-b9g sag12 mutants mirrors the findings of Otegui et al, (2005) and James et al, (2018), who reported knock-out mutants lacking SAG12 function displayed no discernible change in the progression of developmental leaf senescence.…”

Section: The Yellowing Phenotype In the Apex Of Aging Pp2a-b9g Leavessupporting

confidence: 76%

PROTEIN PHOSPHATASE 2A-B′γ Controls Botrytis cinerea Resistance and Developmental Leaf Senescence

et al. 2019

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Plants optimize their growth and survival through highly integrated regulatory networks that coordinate defensive measures and developmental transitions in response to environmental cues. Protein phosphatase 2A (PP2A) is a key signaling component that controls stress reactions and growth at different stages of plant development, and the PP2A regulatory subunit PP2A-B9g is required for negative regulation of pathogenesis responses and for maintenance of cell homeostasis in short-day conditions. Here, we report molecular mechanisms by which PP2A-B9g regulates Botrytis cinerea resistance and leaf senescence in Arabidopsis (Arabidopsis thaliana). We extend the molecular functionality of PP2A-B9g to a protein kinase-phosphatase interaction with the defense-associated calcium-dependent protein kinase CPK1 and present indications this interaction may function to control CPK1 activity. In presenescent leaf tissues, PP2A-B9g is also required to negatively control the expression of salicylic acid-related defense genes, which have recently proven vital in plant resistance to necrotrophic fungal pathogens. In addition, we find the premature leaf yellowing of pp2a-b9g depends on salicylic acid biosynthesis via SALICYLIC ACID INDUCTION DEFICIENT2 and bears the hallmarks of developmental leaf senescence. We propose PP2A-B9g agedependently controls salicylic acid-related signaling in plant immunity and developmental leaf senescence.

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Section: The Yellowing Phenotype In the Apex Of Aging Pp2a-b9g Leavessupporting

confidence: 76%

PROTEIN PHOSPHATASE 2A-B′γ Controls Botrytis cinerea Resistance and Developmental Leaf Senescence

et al. 2019

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“…Otegui et al (2005) showed that a lack of SAG12 did not prevent the formation of senescence associated vacuoles (SAVs), nor was their proteolytic activity affected, suggesting that other cysteine proteases accumulated in SAVs in the senescent leaves of Arabidopsis thaliana (Otegui et al, 2005). More recently, James et al (2018) confirmed the absence of a leaf senescence phenotype in sag12 . The authors also showed that there was no difference in yield and seed N content between Col and sag12 when cultivated under optimal N nutrition, but there was lower seed N content and yield in sag12 when cultivated under limiting nitrogen conditions.…”

Section: Introductionmentioning

confidence: 70%

“…Arabidopsis thaliana Columbia (Col) and sag12 (SALK_124030) T-DNA mutants were used in this study. The KO-SAG12 SALK_124030 ( sag12 ) was chosen because it was the only germplasm which was available in ABRC stock and recently characterized for some study focused on protease activities (Pružinská et al, 2017; James et al, 2018). Seeds were stratified for 48 h in 0.1% agar (Select agar, Sigma, L’Isle d’Abeau Chesnes, France) at 4°C in the dark and then sown into Eppendorf tubes (0.5 ml) filled with 0.8% agar (w/v) that had their bottoms removed.…”

Section: Methodsmentioning

confidence: 99%

“…For all these reasons, a major role for SAG12 in N remobilization during senescence has long been proposed. Surprisingly, no difference in the leaf senescence phenotype between Col and KO-SAG12 ( sag12 ) plants has ever been observed (Otegui et al, 2005; James et al, 2018). Otegui et al (2005) showed that a lack of SAG12 did not prevent the formation of senescence associated vacuoles (SAVs), nor was their proteolytic activity affected, suggesting that other cysteine proteases accumulated in SAVs in the senescent leaves of Arabidopsis thaliana (Otegui et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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A New Role for SAG12 Cysteine Protease in Roots of Arabidopsis thaliana

et al. 2019

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Senescence associated gene (SAG) 12, which encodes a cysteine protease is considered to be important in nitrogen (N) allocation to Arabidopsis thaliana seeds. A decrease in the yield and N content of the seeds was observed in the Arabidopsis SAG12 knockout mutants (sag12) relative to the wild type (Col0) under limited nitrogen nutrition. However, leaf senescence was similar in both lines. To test whether SAG12 is involved in N remobilization from organs other than the leaves, we tested whether root N could be used in N mobilization to the seeds. Root architecture, N uptake capacity and 15N partitioning were compared in the wild type and sag12 under either high nitrogen (HN) or low nitrogen (LN) conditions. No differences in root architecture or root N uptake capacity were observed between the lines under HN or LN. However, under LN conditions, there was an accumulation of 15N in the sag12 roots compared to the wild type with lower allocation of 15N to the seeds. This was accompanied by an increase in root N protein contents and a significant decrease in root cysteine protease activity. SAG12 is expressed in the root stele of the plants at the reproductive stage, particularly under conditions of LN nutrition. Taken together, these results suggest a new role for SAG12. This cysteine protease plays a crucial role in root N remobilization that ensures seed filling and sustains yields when nitrogen availability is low.

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“…A recent study showed that SAG12 knockout Arabidopsis plants did not exhibit any special phenotypic traits when grown under an optimal nitrogen supply. Thus, the gene is involved in Rubisco degradation during the leaf senescence associated with seed filling ( James et al., ). In this study, our results showed that the expression of CsSAG12 in the mature leaves was upregulated by more than 5‐fold (Fig.…”

Section: Discussionmentioning

confidence: 99%

Dynamics of nitrogen translocation from mature leaves to new shoots and related gene expression during spring shoots development in tea plants (Camellia sinensis L.)

Fan

Zhang

Tang

et al. 2020

J. Plant Nutr. Soil Sci.

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The contribution of N remobilization is crucial for new shoots growth and quality formation during spring tea shoots development. However, the translocation mechanism of N from source leaves to sink young shoots is not well understood. In the present study, 15N urea was applied to mature tea leaves one week before bud break to track N remobilization in a field experiment. The dynamic changes in plant 15N abundance, contents of amino acids, and the expression levels of genes related to N metabolism and translocation were followed during the 18‐d development of new spring shoots until three expanding young leaves. The results showed that during the growth of new shoots the amount of 15N in the shoots increased, whereas the Ndff (N derived from 15N‐urea) in mature leaves decreased, showing that the foliar‐applied N in mature leaves was readily exported to new shoots. This process was found to be accompanied by decline of chlorophylls. In the mature leaves, expression CsATG18a and CsSAG12 involved in autophagy was dramatically induced (> 4‐fold) at approximately nine days after the bud breaking. The genes involved in the transformation of amino acids, including primarily CsGDH2, CsGDH4, CsGLT3, CsGS1;3, and CsASN2 were upregulated by > 3‐fold after bud breaking. The expression levels of CsATG8A, CsATG9, CsSAG12, CsGS1;1, CsGDH1, and CsAAP6 correlated negatively with the Ndff in mature leaves, but positively with 15N amount and total N amount in new shoots, suggesting these genes played important roles in N export from mature leaves. In the new shoots, the expression of most genes showed two defined peaks, one on six days and one on 12 days after bud breaking. The expression of CsGS2, CsASN3, CsGLT1, and CsAAP4 positively correlated with the 15N amount and total N amount in new shoots. These genes might be involved in the transport and re‐assimilation of N from mature leaves. The overall results demonstrated that the translocation of 15N from mature leaves to new spring shoots was regulated by the genes involved in autophagy, protein degradation, amino acid transformation and transport.

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SAG12, a Major Cysteine Protease Involved in Nitrogen Allocation during Senescence for Seed Production in Arabidopsis thaliana

Cited by 75 publications

References 51 publications

PROTEIN PHOSPHATASE 2A-B′γ Controls Botrytis cinerea Resistance and Developmental Leaf Senescence

PROTEIN PHOSPHATASE 2A-B′γ Controls Botrytis cinerea Resistance and Developmental Leaf Senescence

A New Role for SAG12 Cysteine Protease in Roots of Arabidopsis thaliana

Dynamics of nitrogen translocation from mature leaves to new shoots and related gene expression during spring shoots development in tea plants (Camellia sinensis L.)

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