PDX proteins from Arabidopsis thaliana as novel substrates of cathepsin B: implications for vitamin B 6 biosynthesis regulation.

Publisher: Published by Blackwell Pub. on behalf of the Federation of European Biochemical Societies Country of Publication: England NLM ID: 101229646 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1742-4658 (Electronic) Linking ISSN: 1742464X NLM ISO Abbreviation: FEBS J Subsets: MEDLINE

Original Publication: Oxford, UK : Published by Blackwell Pub. on behalf of the Federation of European Biochemical Societies, c2005-

Arabidopsis*/metabolism ; Arabidopsis*/genetics ; Arabidopsis Proteins*/metabolism ; Arabidopsis Proteins*/genetics ; Cathepsin B*/metabolism ; Cathepsin B*/genetics ; Vitamin B 6*/metabolism ; Vitamin B 6*/biosynthesis; Carbon-Nitrogen Lyases/genetics ; Carbon-Nitrogen Lyases/metabolism ; Gene Expression Regulation, Plant ; Substrate Specificity ; Ubiquitination ; Nitrogenous Group Transferases/genetics ; Nitrogenous Group Transferases/metabolism

Vitamin B 6 is a critical molecule for metabolism, development, and stress sensitivity in plants. It is a cofactor for numerous biochemical reactions, can serve as an antioxidant, and has the potential to increase tolerance against both biotic and abiotic stressors. Due to the importance of vitamin B 6 , its biosynthesis is likely tightly regulated. Plants can synthesize vitamin B 6 de novo via the concerted activity of Pyridoxine Biosynthesis Protein 1 (PDX1) and PDX2. Previously, PDX proteins have been identified as targets for ubiquitination, indicating they could be marked for degradation by two highly conserved pathways: the Ubiquitin Proteasome Pathway (UPP) and the autophagy pathway. Initial experiments show that PDXs are in fact degraded, but surprisingly, in a ubiquitin-independent manner. Inhibitor studies pointed toward cathepsin B, a conserved lysosomal cysteine protease, which is implicated in both programed cell death and autophagy in humans and plants. In plants, cathepsin Bs are poorly described, and no confirmed substrates have been identified. Here, we present PDX proteins from Arabidopsis thaliana as interactors and substrates of a plant Cathepsin B. These findings not only describe a novel cathepsin B substrate in plants, but also provide new insights into how plants regulate de novo biosynthesis of vitamin B 6 .
(© 2024 Federation of European Biochemical Societies.)

Parra M, Stahl S & Hellmann H (2018) Vitamin B6 and its role in cell metabolism and physiology. Cell 7, 84.
Bilski P, Li MY, Ehrenshaft M, Daub ME & Chignell CF (2000) Vitamin B6 (pyridoxine) and its derivatives are efficient singlet oxygen quenchers and potential fungal antioxidants. Photochem Photobiol 71, 129–134.
Bagri DS, Upadhyaya DC, Kumar A & Upadhyaya CP (2018) Overexpression of PDX‐II gene in potato (Solanum tuberosum L.) leads to the enhanced accumulation of vitamin B6 in tuber tissues and tolerance to abiotic stresses. Plant Sci 272, 267–275.
Titiz O, Tambasco‐Studart M, Warzych E, Apel K, Amrhein N, Laloi C & Fitzpatrick TB (2006) PDX1 is essential for vitamin B6 biosynthesis, development and stress tolerance in Arabidopsis. Plant J 48, 933–946.
Nan N, Wang J, Shi Y, Qian Y, Jiang L, Huang S, Liu Y, Wu Y, Liu B & Xu Z‐Y (2020) Rice plastidial NAD‐dependent malate dehydrogenase 1 negatively regulates salt stress response by reducing the vitamin B6 content. Plant Biotechnol J 18, 172–184.
Liu Y, Maniero RA, Giehl RFH, Melzer M, Steensma P, Krouk G, Fitzpatrick TB & von Wirén N (2022) PDX1.1‐dependent biosynthesis of vitamin B6 protects roots from ammonium‐induced oxidative stress. Mol Plant 15, 820–839.
Brin M (1970) A simplified Toepfer‐Lehmann assay for the three vitamin B6 vitamers. In Methods in Enzymology (Mccormick DB & Wright LD, eds), pp. 519–523. Academic Press, New York, NY.
Rabinowitz JC & Snell EE (1948) The vitamin B6 group, distribution of pyridoxal, pyridoxamine, and pyridoxine in some natural products. J Biol Chem 176, 1157–1167.
Heyl D, Luz E, Harris SA & Folkers K (1951) Phosphates of the vitamin B6 group. I. The structure of codecarboxylase. J Am Chem Soc 73, 3430–3433.
Ploux O & Marquet A (1996) Mechanistic studies on the 8‐amino‐7‐oxopelargonate synthase, a pyridoxal‐5′‐phosphate‐dependent enzyme involved in biotin biosynthesis. Eur J Biochem 236, 301–308.
Shaw JP, Petsko GA & Ringe D (1997) Determination of the structure of alanine racemase from Bacillus stearothermophilus at 1.9‐A resolution. Biochemistry 36, 1329–1342.
Sun S, Zabinski RF & Toney MD (1998) Reactions of alternate substrates demonstrate stereoelectronic control of reactivity in dialkylglycine decarboxylase. Biochemistry 37, 3865–3875.
Guédez G, Hipp K, Windeisen V, Derrer B, Gengenbacher M, Böttcher B, Sinning I, Kappes B & Tews I (2012) Assembly of the eukaryotic PLP‐synthase complex from Plasmodium and activation of the Pdx1 enzyme. Structure 20, 172–184.
Strohmeier M, Raschle T, Mazurkiewicz J, Rippe K, Sinning I, Fitzpatrick TB & Tews I (2006) Structure of a bacterial pyridoxal 5′‐phosphate synthase complex. Proc Natl Acad Sci USA 103, 19284–19289.
Zhu J, Burgner JW, Harms E, Belitsky BR & Smith JL (2005) A new arrangement of (beta/alpha)8 barrels in the synthase subunit of PLP synthase. J Biol Chem 280, 27914–27923.
Tambasco‐Studart M, Titiz O, Raschle T, Forster G, Amrhein N & Fitzpatrick TB (2005) Vitamin B6 biosynthesis in higher plants. Proc Natl Acad Sci USA 102, 13687–13692.
Chen H & Xiong L (2005) Pyridoxine is required for post‐embryonic root development and tolerance to osmotic and oxidative stresses. Plant J 44, 396–408.
Wagner S, Bernhardt A, Leuendorf JE, Drewke C, Lytovchenko A, Mujahed N, Gurgui C, Frommer WB, Leistner E, Fernie AR et al. (2006) Analysis of the Arabidopsis rsr4‐1/pdx1‐3 mutant reveals the critical function of the PDX1 protein family in metabolism, development, and vitamin B6 biosynthesis. Plant Cell 18, 1722–1735.
Moccand C, Boycheva S, Surriabre P, Tambasco‐Studart M, Raschke M, Kaufmann M & Fitzpatrick TB (2014) The pseudoenzyme PDX1.2 boosts vitamin B6 biosynthesis under heat and oxidative stress in Arabidopsis. J Biol Chem 289, 8203–8216.
Dell'Aglio E, Dalvit I, Loubéry S & Fitzpatrick TB (2019) Clarification of the dispensability of PDX1.2 for Arabidopsis viability using CRISPR/Cas9. BMC Plant Biol 19, 464.
Novikova IV, Zhou M, Du C, Parra M, Kim DN, VanAernum ZL, Shaw JB, Hellmann H, Wysocki VH & Evans JE (2021) Tunable heteroassembly of a plant pseudoenzyme–enzyme complex. ACS Chem Biol 16, 2315–2325.
Denslow SA, Rueschhoff EE & Daub ME (2007) Regulation of the Arabidopsis thaliana vitamin B6 biosynthesis genes by abiotic stress. Plant Physiol Biochem 45, 152–161.
Manzano C, Abraham Z, López‐Torrejón G & Del Pozo JC (2008) Identification of ubiquitinated proteins in Arabidopsis. Plant Mol Biol 68, 145–158.
Saracco SA, Hansson M, Scalf M, Walker JM, Smith LM & Vierstra RD (2009) Tandem affinity purification and mass spectrometric analysis of ubiquitylated proteins in Arabidopsis. Plant J 59, 344–358.
Smalley S & Hellmann H (2022) Review: exploring possible approaches using ubiquitylation and sumoylation pathways in modifying plant stress tolerance. Plant Sci 319, 111275.
Su T, Yang M, Wang P, Zhao Y & Ma C (2020) Interplay between the ubiquitin proteasome system and ubiquitin‐mediated autophagy in plants. Cell 9, 2219.
Livneh I, Cohen‐Kaplan V, Cohen‐Rosenzweig C, Avni N & Ciechanover A (2016) The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death. Cell Res 26, 869–885.
Genschik P (2019) RPN10: a case study for ubiquitin binding proteins and more. Plant Cell 31, 1398–1399.
Al‐Saharin R, Hellmann H & Mooney S (2022) Plant E3 ligases and their role in abiotic stress response. Cell 11, 890.
Kim PK, Hailey DW, Mullen RT & Lippincott‐Schwartz J (2008) Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci USA 105, 20567–20574.
Kirkin V, Lamark T, Sou Y‐S, Bjørkøy G, Nunn JL, Bruun J‐A, Shvets E, McEwan DG, Clausen TH, Wild P et al. (2009) A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 33, 505–516.
Leong JX, Raffeiner M, Spinti D, Langin G, Franz‐Wachtel M, Guzman AR, Kim J‐G, Pandey P, Minina AE, Macek B et al. (2022) A bacterial effector counteracts host autophagy by promoting degradation of an autophagy component. EMBO J 41, e110352.
Qi H, Li J, Xia F‐N, Chen J‐Y, Lei X, Han M‐Q, Xie L‐J, Zhou Q‐M & Xiao S (2020) Arabidopsis SINAT proteins control autophagy by mediating ubiquitylation and degradation of ATG13. Plant Cell 32, 263–284.
Wang P, Nolan TM, Clark NM, Jiang H, Montes‐Serey C, Guo H, Bassham DC, Walley JW & Yin Y (2021) The F‐box E3 ubiquitin ligase BAF1 mediates the degradation of the brassinosteroid‐activated transcription factor BES1 through selective autophagy in Arabidopsis. Plant Cell 33, 3532–3554.
Zhang T, Xiao Z, Liu C, Yang C, Li J, Li H, Gao C & Shen W (2021) Autophagy mediates the degradation of plant ESCRT component FREE1 in response to iron deficiency. Int J Mol Sci 22, 8779.
Su T, Li X, Yang M, Shao Q, Zhao Y, Ma C & Wang P (2020) Autophagy: an intracellular degradation pathway regulating plant survival and stress response. Front Plant Sci 11, 164.
Le Bars R, Marion J, Le Borgne R, Satiat‐Jeunemaitre B & Bianchi MW (2014) ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants. Nat Commun 5, 4121.
Marshall RS & Vierstra RD (2018) Autophagy: the master of bulk and selective recycling. Annu Rev Plant Biol 69, 173–208.
Wang P, Mugume Y & Bassham DC (2018) New advances in autophagy in plants: regulation, selectivity and function. Semin Cell Dev Biol 80, 113–122.
Young PG, Passalacqua MJ, Chappell K, Llinas RJ & Bartel B (2019) A facile forward‐genetic screen for Arabidopsis autophagy mutants reveals twenty‐one loss‐of‐function mutations disrupting six ATG genes. Autophagy 15, 941–959.
Marty F (1999) Plant vacuoles. Plant Cell 11, 587–599.
Turk V, Stoka V, Vasiljeva O, Renko M, Sun T, Turk B & Turk D (2012) Cysteine cathepsins: from structure, function and regulation to new frontiers. Biochim Biophys Acta 1824, 68–88.
Brix K, Dunkhorst A, Mayer K & Jordans S (2008) Cysteine cathepsins: cellular roadmap to different functions. Biochimie 90, 194–207.
Patel S, Homaei A, El‐Seedi HR & Akhtar N (2018) Cathepsins: proteases that are vital for survival but can also be fatal. Biomed Pharmacother 105, 526–532.
Illy C, Quraishi O, Wang J, Purisima E, Vernet T & Mort JS (1997) Role of the occluding loop in cathepsin B activity. J Biol Chem 272, 1197–1202.
Nägler DK, Storer AC, Portaro FCV, Carmona E, Juliano L & Ménard R (1997) Major increase in endopeptidase activity of human cathepsin B upon removal of occluding loop contacts. Biochemistry 36, 12608–12615.
Redzynia I, Ljunggren A, Abrahamson M, Mort JS, Krupa JC, Jaskolski M & Bujacz G (2008) Displacement of the occluding loop by the parasite protein, chagasin, results in efficient inhibition of human cathepsin B. J Biol Chem 283, 22815–22825.
Porodko A, Cirnski A, Petrov D, Raab T, Paireder M, Mayer B, Maresch D, Nika L, Biniossek ML, Gallois P et al. (2018) The two cathepsin B‐like proteases of Arabidopsis thaliana are closely related enzymes with discrete endopeptidase and carboxydipeptidase activities. Biol Chem 399, 1223–1235.
Cai Y‐M, Yu J, Ge Y, Mironov A & Gallois P (2018) Two proteases with caspase‐3‐like activity, cathepsin B and proteasome, antagonistically control ER‐stress‐induced programmed cell death in Arabidopsis. New Phytol 218, 1143–1155.
Chen G, Zhang D, Pan J, Yue J & Shen X (2021) Cathepsin B‐like cysteine protease ApCathB negatively regulates cryo‐injury tolerance in transgenic Arabidopsis and Agapanthus praecox. Plant Sci 308, 110928.
Minina EA, Bozhkov PV & Hofius D (2014) Autophagy as initiator or executioner of cell death. Trends Plant Sci 19, 692–697.
Bárány I, Berenguer E, Solís M‐T, Pérez‐Pérez Y, Santamaría ME, Crespo JL, Risueño MC, Díaz I & Testillano PS (2018) Autophagy is activated and involved in cell death with participation of cathepsins during stress‐induced microspore embryogenesis in barley. J Exp Bot 69, 1387–1402.
Kim D‐Y, Scalf M, Smith LM & Vierstra RD (2013) Advanced proteomic analyses yield a deep catalog of ubiquitylation targets in Arabidopsis. Plant Cell 25, 1523–1540.
Spence J, Sadis S, Haas AL & Finley D (1995) A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol Cell Biol 15, 1265–1273.
Dimkovikj A, Fisher B, Hutchison K & Van Hoewyk D (2015) Stuck between a ROS and a hard place: analysis of the ubiquitin proteasome pathway in selenocysteine treated Brassica napus reveals different toxicities during selenium assimilation. J Plant Physiol 181, 50–54.
Tokumaru M, Adachi F, Toda M, Ito‐Inaba Y, Yazu F, Hirosawa Y, Sakakibara Y, Suiko M, Kakizaki T & Inaba T (2017) Ubiquitin‐proteasome dependent regulation of the GOLDEN2‐LIKE 1 transcription factor in response to plastid signals. Plant Physiol 173, 524–535.
Wang J, Qin H, Zhou S, Wei P, Zhang H, Zhou Y, Miao Y & Huang R (2020) The ubiquitin‐binding protein OsDSK2a mediates seedling growth and salt responses by regulating gibberellin metabolism in rice. Plant Cell 32, 414–428.
Letoha T, Somlai C, Takács T, Szabolcs A, Rakonczay Z, Jármay K, Szalontai T, Varga I, Kaszaki J, Boros I et al. (2005) The proteasome inhibitor MG132 protects against acute pancreatitis. Free Radic Biol Med 39, 1142–1151.
Ma C, Sacco MD, Hurst B, Townsend JA, Hu Y, Szeto T, Zhang X, Tarbet B, Marty MT, Chen Y et al. (2020) Boceprevir, GC‐376, and calpain inhibitors II, XII inhibit SARS‐CoV‐2 viral replication by targeting the viral main protease. Cell Res 30, 678–692.
Ost GS, Ng'ang'a PN, Lang AE & Aktories K (2019) Photorhabdus luminescens Tc toxin is inhibited by the protease inhibitor MG132 and activated by protease cleavage resulting in increased binding to target cells. Cell Microbiol 21, e12978.
Johnson KL, Faulkner C, Jeffree CE & Ingram GC (2008) The phytocalpain defective kernel 1 is a novel Arabidopsis growth regulator whose activity is regulated by proteolytic processing. Plant Cell 20, 2619–2630.
McLellan H, Gilroy EM, Yun B‐W, Birch PRJ & Loake GJ (2009) Functional redundancy in the Arabidopsis cathepsin B gene family contributes to basal defence, the hypersensitive response and senescence. New Phytol 183, 408–418.
Berkers CR, Verdoes M, Lichtman E, Fiebiger E, Kessler BM, Anderson KC, Ploegh HL, Ovaa H & Galardy PJ (2005) Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib. Nat Methods 2, 357–362.
Oliveira SSC, Gonçalves IC, Ennes‐Vidal V, Lopes AHCS, Menna‐Barreto RFS, D'ávila‐Levy CM, Santos ALS & Branquinha MH (2018) In vitro selection of Phytomonas serpens cells resistant to the calpain inhibitor MDL28170: alterations in fitness and expression of the major peptidases and efflux pumps. Parasitology 145, 355–370.
Templeman NM, Luo S, Kaletsky R, Shi C, Ashraf J, Keyes W & Murphy CT (2018) Insulin signaling regulates oocyte quality maintenance with age via cathepsin B activity. Curr Biol 28, 753–760.e4.
Buttle DJ, Murata M, Knight CG & Barrett AJ (1992) CA074 methyl ester: a proinhibitor for intracellular cathepsin B. Arch Biochem Biophys 299, 377–380.
Tsuji A, Kikuchi Y, Ogawa K, Saika H, Yuasa K & Nagahama M (2008) Purification and characterization of cathepsin B‐like cysteine protease from cotyledons of daikon radish, Raphanus sativus. FEBS J 275, 5429–5443.
Niemer M, Mehofer U, Verdianz M, Porodko A, Schähs P, Kracher D, Lenarcic B, Novinec M & Mach L (2016) Nicotiana benthamiana cathepsin B displays distinct enzymatic features which differ from its human relative and aleurain‐like protease. Biochimie 122, 119–125.
Ge Y, Cai Y‐M, Bonneau L, Rotari V, Danon A, McKenzie EA, McLellan H, Mach L & Gallois P (2016) Inhibition of cathepsin B by caspase‐3 inhibitors blocks programmed cell death in Arabidopsis. Cell Death Differ 23, 1493–1501.
Leuendorf JE, Osorio S, Szewczyk A, Fernie AR & Hellmann H (2010) Complex assembly and metabolic profiling of Arabidopsis thaliana plants overexpressing vitamin B6 biosynthesis proteins. Mol Plant 3, 890–903.
Castro PH, Verde N, Lourenço T, Magalhães AP, Tavares RM, Bejarano ER & Azevedo H (2015) SIZ1‐dependent post‐translational modification by SUMO modulates sugar signaling and metabolism in Arabidopsis thaliana. Plant Cell Physiol 56, 2297–2311.
Belloni D, Veschini L, Foglieni C, Dell'Antonio G, Caligaris‐Cappio F, Ferrarini M & Ferrero E (2010) Bortezomib induces autophagic death in proliferating human endothelial cells. Exp Cell Res 316, 1010–1018.
Williams JA, Hou Y, Ni H‐M & Ding W‐X (2013) Role of intracellular calcium in proteasome inhibitor‐induced endoplasmic reticulum stress, autophagy, and cell death. Pharm Res 30, 2279–2289.
Wipf P & Halter RJ (2005) Chemistry and biology of wortmannin. Org Biomol Chem 3, 2053–2061.
Blommaart EFC, Krause U, Schellens JPM, Vreeling‐Sindelárová H & Meijer AJ (1997) The phosphatidylinositol 3‐kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243, 240–246.
Pasquier B (2016) Autophagy inhibitors. Cell Mol Life Sci 73, 985–1001.
van Wijk KJ, Leppert T, Sun Z & Deutsch EW (2023) Does the ubiquitination degradation pathway really reach inside of the chloroplast? A re‐evaluation of mass spectrometry‐based assignments of ubiquitination. J Proteome Res 22, 2079–2091.
Bose K JC, Kapoor BS, Mandal K, Ghosh S, Mokhamatam RB, Manna SK & Mukhopadhyay SS (2020) Loss of mitochondrial localization of human FANCG causes defective FANCJ helicase. Mol Cell Biol 40, e00306‐20.
Chen H, Feng H, Zhang X, Zhang C, Wang T & Dong J (2019) An Arabidopsis E3 ligase HUB2 increases histone H2B monoubiquitination and enhances drought tolerance in transgenic cotton. Plant Biotechnol J 17, 556–568.
Barberon M, Zelazny E, Robert S, Conéjéro G, Curie C, Friml J & Vert G (2011) Monoubiquitin‐dependent endocytosis of the IRON‐REGULATED TRANSPORTER 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108, E450–E458.
Romero‐Barrios N & Vert G (2018) Proteasome‐independent functions of lysine‐63 polyubiquitination in plants. New Phytol 217, 995–1011.
Yau R & Rape M (2016) The increasing complexity of the ubiquitin code. Nat Cell Biol 18, 579–586.
Swatek KN & Komander D (2016) Ubiquitin modifications. Cell Res 26, 399–422.
Chen Q, Shinozaki D, Luo J, Pottier M, Havé M, Marmagne A, Reisdorf‐Cren M, Chardon F, Thomine S, Yoshimoto K et al. (2019) Autophagy and nutrients management in plants. Cell 8, 1426.
Thompson AR, Doelling JH, Suttangkakul A & Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138, 2097–2110.
Mooney S, Leuendorf J‐E, Hendrickson C & Hellmann H (2009) Vitamin B6: a long known compound of surprising complexity. Molecules 14, 329–351.
Bernard SM & Habash DZ (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182, 608–620.
Fernie AR, Carrari F & Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 7, 254–261.
Kopp J, Kopriva S, Süss K‐H & Schulz GE (1999) Structure and mechanism of the amphibolic enzyme d‐ribulose‐5‐phosphate 3‐epimerase from potato chloroplasts. J Mol Biol 287, 761–771.
Li Y, Peng L, Wang X & Zhang L (2022) Reduction in chloroplastic ribulose‐5‐phosphate‐3‐epimerase decreases photosynthetic capacity in Arabidopsis. Front Plant Sci 13, 813241.
Henry E, Fung N, Liu J, Drakakaki G & Coaker G (2015) Beyond glycolysis: GAPDHs are multi‐functional enzymes involved in regulation of ROS, autophagy, and plant immune responses. PLoS Genet 11, e1005199.
Mangel N, Fudge JB, Li K‐T, Wu T‐Y, Tohge T, Fernie AR, Szurek B, Fitzpatrick TB, Gruissem W & Vanderschuren H (2019) Enhancement of vitamin B6 levels in rice expressing Arabidopsis vitamin B6 biosynthesis de novo genes. Plant J 99, 1047–1065.
Dell'Aglio E, Boycheva S & Fitzpatrick TB (2017) The pseudoenzyme PDX1.2 sustains vitamin B6 biosynthesis as a function of heat stress. Plant Physiol 174, 2098–2112.
Vanderschuren H, Boycheva S, Li K‐T, Szydlowski N, Gruissem W & Fitzpatrick T (2013) Strategies for vitamin B6 biofortification of plants: a dual role as a micronutrient and a stress protectant. Front Plant Sci 4, 143.
Herrero S, González E, Gillikin JW, Vélëz H & Daub ME (2011) Identification and characterization of a pyridoxal reductase involved in the vitamin B6 salvage pathway in Arabidopsis. Plant Mol Biol 76, 157–169.
Chen H, Dong J & Wang T (2021) Autophagy in plant abiotic stress management. Int J Mol Sci 22, 4075.
Czégény G, Kőrösi L, Strid Å & Hideg É (2019) Multiple roles for vitamin B6 in plant acclimation to UV‐B. Sci Rep 9, 1259.
Hörger AC & van der Hoorn RA (2013) The structural basis of specific protease–inhibitor interactions at the plant–pathogen interface. Curr Opin Struct Biol 23, 842–850.
Yoon MC, Christy MP, Phan VV, Gerwick WH, Hook G, O'Donoghue AJ & Hook V (2022) Molecular features of CA‐074 pH‐dependent inhibition of cathepsin B. Biochemistry 61, 228–238.
Lohman KN, Gan S, John MC & Amasino RM (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92, 322–328.
Pružinská A, Shindo T, Niessen S, Kaschani F, Tóth R, Millar AH & van der Hoorn RAL (2017) Major Cys protease activities are not essential for senescence in individually darkened Arabidopsis leaves. BMC Plant Biol 17, 4.
Masclaux‐Daubresse C, Chen Q & Havé M (2017) Regulation of nutrient recycling via autophagy. Curr Opin Plant Biol 39, 8–17.
Havé M, Marmagne A, Chardon F & Masclaux‐Daubresse C (2017) Nitrogen remobilization during leaf senescence: lessons from Arabidopsis to crops. J Exp Bot 68, 2513–2529.
Havé M, Balliau T, Cottyn‐Boitte B, Dérond E, Cueff G, Soulay F, Lornac A, Reichman P, Dissmeyer N, Avice J‐C et al. (2018) Increases in activity of proteasome and papain‐like cysteine protease in Arabidopsis autophagy mutants: back‐up compensatory effect or cell‐death promoting effect? J Exp Bot 69, 1369–1385.
Estelle MA & Somerville C (1987) Auxin‐resistant mutants of Arabidopsis thaliana with an altered morphology. Mol Gen Genet 206, 200–206.
Wang F, Zhu D, Huang X, Li S, Gong Y, Yao Q, Fu X, Fan L‐M & Deng XW (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell‐free assay system. Plant Cell 21, 2378–2390.
Biedermann S & Hellmann H (2010) The DDB1a interacting proteins ATCSA‐1 and DDB2 are critical factors for UV‐B tolerance and genomic integrity in Arabidopsis thaliana. Plant J 62, 404–415.
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein‐dye binding. Anal Biochem 72, 248–254.
Schindelin J, Arganda‐Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B et al. (2012) Fiji: an open‐source platform for biological‐image analysis. Nat Methods 9, 676–682.

BB/T008725/1 BBSRC DTP3 competitive grant

Keywords: cathepsin B; metabolism; pyridoxin; regulation; vitamin B6

0 (Arabidopsis Proteins)
EC 4.3.3.6 (At2g38230 protein, Arabidopsis)
EC 4.3.- (Carbon-Nitrogen Lyases)
EC 3.4.22.1 (Cathepsin B)
8059-24-3 (Vitamin B 6)
EC 2.6.- (PDX2 protein, Arabidopsis)
EC 2.6.- (Nitrogenous Group Transferases)

Date Created: 20240303 Date Completed: 20240605 Latest Revision: 20241021

20250114

10.1111/febs.17110

38431778