PLANT SIGNALING & BEHAVIOR 2016, VOL. 11, NO. 10, e1231293 (3 pages) http://dx.doi.org/10.1080/15592324.2016.1231293

ARTICLE ADDENDUM

NatA is required for suspensor development in Arabidopsis Jinlin Fenga,b and Ligeng Maa a

College of Life Sciences, Capital Normal University, Beijing, China; bCollege of Life Sciences, Shanxi Normal University, Linfen, Shanxi, China

ABSTRACT

Suspensor development is essential for early embryogenesis. The filamentous suspensor plays vital roles in supporting the embryo proper and in exchanging nutrients and information between the embryo proper and embryo sac. In addition, at the globular stage, the uppermost suspensor cell differentiates into the hypophysis, which generates the progenitors of the quiescent center and columella stem cells. In naa10 and naa15 mutant plants, suspensor cell identity was found to be abnormal and embryo development was disturbed, leading to embryonic lethality. Therefore, the NatA complex is required for proper suspensor development in Arabidopsis.

Embryogenesis is the onset of the next generation. Cell division and differentiation within the embryo proper and suspensor are regulated by both an internal genetic program and environmental signals.1,2 Polar auxin distribution, established by auxin transporters called PINs, is essential for embryogenesis.3 Defects in auxin responses, perception, transport, or biogenesis can cause defects in embryogenesis and embryo formation.4-9 The suspensor, which is derived from the basal cell of a 2celled proembryo, is a unique embryonic region that connects the embryo and seed coat.10-12 Through horizontal division of the basal cell, the filamentous suspensor contains an enlarged bottom cell, which is attached to maternal tissues, and a single row of 6 to 8 additional cells.13 The suspensor becomes highly differentiated early in development and then degenerates during the subsequent cotyledon stage of embryogenesis.12,13 The suspensor plays an important role in embryo development; it transfers nutrients and growth factors to the embryo proper and biosynthesizes plant hormones.12,14,15 For example, auxin is transported from the suspensor to the embryo proper by the suspensor-specific auxin efflux carrier PIN7, and PIN7mediated auxin transport is essential for embryo development.16,17 The suspensor is also important for pushing the embryo into the lumen of the seed, where the embryo is surrounded by the nourishing endosperm.18 Thus, in Arabidopsis the length and structure of the suspensor are crucial for the fast developmental progression of an embryo.18 Suspensor cells also have embryogenic potential, which is suppressed by the embryo proper during normal embryogenesis.19 Following embryo removal, auxin gradually accumulates in the top suspensor cell, where cell division occurs to produce a new embryo.19 Therefore, auxin redistribution appears to reprogram the fate of the suspensor cell and triggers embryogenesis in suspensor cells. We previously found that mutation of the catalytic subunit (Naa10) or auxiliary subunit (Naa15) of NatA caused an

ARTICLE HISTORY

Received 16 August 2016 Revised 28 August 2016 Accepted 29 August 2016 KEYWORDS

Arabidopsis; embryo proper; NatA; protein N-terminal acetylation; suspensor

embryo-lethal phenotype and that NatA was required for the proper patterning of lower-tier cells, upper-tier cells, and the entire embryo.20 In the present work, we found that NatA is also required for suspensor development during embryogenesis in Arabidopsis. In wild-type plants, the square-like 8-celled filamentous suspensor was observed to be regularly arranged and tightly linked with neighboring cells; this produced a tough suspensor and ensured placement of the embryo proper in the seed lumen at the globular stage [4 d after pollination (DAP)] (Fig. 1A). The structure of the suspensor was normal but development was delayed in naa10 and naa15 mutants compared with wild-type plants at 4 DAP (Fig. 1B–D). Mature wild-type embryos without a clear suspensor cell were noted at 9 DAP (Fig. 1E); this may have been caused by the programmed cell death of suspensor cells.21 In contrast, naa10 and naa15 mutant embryos contained a suspensor with enlarged cells (Fig. 1G and H) compared to wild-type suspensors at the same (Fig. 1A) or a later (Fig. 1F) developmental stage. Suspensor toughness in the mutants was reduced due to the morphologically abnormal suspensor cells; this resulted in a slant in the embryo proper in the seed lumen (Fig. 1G and H). These results indicate that the NatA complex is required for proper suspensor development during embryogenesis in Arabidopsis. Although it was discovered decades ago, the function of Nterminal acetylation is poorly understood.22 Several key findings suggest that N-terminal acetylation is involved in protein stability,23 protein interactions,24 plant responses to pathogens,25 and drought stress.26 The NatA complex is an N-terminal acetyltransferase complex that acetylates Ser, Ala, Thr, Gly, Val, or Cys residues within the N-terminus of a peptide after the initiator methionine is removed by methionine aminopeptidase.27,28,29,30 Therefore, the NatA complex establishes a link between cellular metabolism and the regulation of protein

CONTACT Ligeng Ma [email protected] Addendum to: Feng J, Li R, Yu J, Ma S, Wu C, Li Y, Cao Y, Ma L. Protein N-terminal Acetylation Is Required for Embryogenesis in Arabidopsis; J Exp Bot. 2016 Aug;67(15): 4779-89; http://dx.doi.org/10.1093/jxb/erw257 © 2016 Taylor & Francis Group, LLC

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J. FENG AND L. MA

Figure 1. NatA is required for suspensor identity in Arabidopsis. Cleared wild-type embryos at the globular (A) and dermatogen (B) stages, and naa10-1 (C) and naa15-3 (D) embryos at the dermatogen stage, are shown. Cleared wild-type embryos at the mature (E) and heart (F) stages, and naa10-1 (G) and naa15-3 (H) embryos at a globular-like stage, are shown. DAP: days after pollination. Scale bar D 20 mm.

function. In the present and previous reports, we found that the NatA complex was required for early embryogenesis and suspensor development,20 indicating that protein N-terminal acetylation is essential for embryogenesis in Arabidopsis. However, the direct targets of NatA in Arabidopsis are unknown. Table 1 summarizes the proteins that are involved in embryogenesis Table 1. Predicted substrates of NatA that are involved in embryogenesis and suspensor development. Protein

N-terminal sequence (first 20 amino acid residues)

Predicted N-terminal acetylation site

Likelihood (%)

ARF9 TOM7 SCR TOAD2 WOX9 WOX8 WOX5 TPL NUP62 ACC1 TAF6 ISE1 ALT2 RIE1 CDF1 PEX19B PEX19A SMO2-1 THA8 TWN2

MANRGGEYLYDELWKLCAGP MAAKSTLKIKGKAKPSKGSS MAESGDFNGGQPPPHSPLRT MTSLPSSVIKWRFFRRQMPS MASSNRHWPSMFKSKPHPHQ MSSSNKNWPSMFKSKPCNNN MSFSVKGRSLRGNNNGGTGT MSSLSRELVFLILQFLDEEK MSGFPFGQSNSVGGFSFGSS MAGSVNGNHSAVGPGINYET MSIVPKETVEVIAQSIGITN MAASTSTRFLVLLKDFSAFR MSKRPPPDPVAVLRGHRHSV MSSYSSDSTAARDQHAPLLR MSSSLLLSGSTVSSSFIAPS MANDTHTDDLDELLDSALDD MANSHTDDLDELLDSALDDF MASFVESGWQYLVTHFSDFQ MALSLSQTRPPSLSHSHTLS MSLLFLRRAKPLFVSCCSAT

Ac-A (2) Ac-A (2) Ac-A (2) Ac-T (2) Ac-A (2) Ac-S (2) Ac-S (2) Ac-S (2) Ac-S (2) Ac-A (2) Ac-S (2) Ac-A (2) Ac-S (2) Ac-S (2) Ac-S (2) Ac-A (2) Ac-A (2) Ac-A (2) Ac-A (2) Ac-S (2)

83 83 83 77 83 85 85 85 85 83 85 83 85 85 85 83 83 83 83 85

and suspensor development, and which are predicted to be substrates of NatA in Arabidopsis (https://bioweb.i2bc.parissaclay.fr/terminator3/). It would be interesting to verify whether any of the proteins in Table 1 is targeted for acetylation by NatA in Arabidopsis.

Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.

Acknowledgments We thank Dr. Jessica Habashi for critical reading of the manuscript.

Funding This work was supported by grant from the Beijing Municipal Government Science Foundation (CIT&TCD20150102) and Natural Science Foundation of China (31600248).

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NatA is required for suspensor development in Arabidopsis.

Suspensor development is essential for early embryogenesis. The filamentous suspensor plays vital roles in supporting the embryo proper and in exchang...
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