Delayed leaf greening involves a major shift in the expression of cytosolic and mitochondrial ribosomes to plastid ribosomes in the highly phosphorus-use-efficient Hakea prostrata (Proteaceae)

Bird, T; Nestor, BJ; Bayer, PE; Wang, G; Ilyasova, A; Gille, CE; Soraru, BEH; Ranathunge, K; Severn-Ellis, AA; Jost, Ricarda; Scheible, WR; Dassanayake, M; Batley, J; Edwards, D; Lambers, H; Finnegan, PM

doi:10.26181/25538347.v1

1381172_Bird,T_2024.pdf (3.32 MB)

Delayed leaf greening involves a major shift in the expression of cytosolic and mitochondrial ribosomes to plastid ribosomes in the highly phosphorus-use-efficient Hakea prostrata (Proteaceae)

journal contribution

posted on 2024-04-04, 02:31 authored by T Bird, BJ Nestor, PE Bayer, G Wang, A Ilyasova, CE Gille, BEH Soraru, K Ranathunge, AA Severn-Ellis, Ricarda JostRicarda Jost, WR Scheible, M Dassanayake, J Batley, D Edwards, H Lambers, PM Finnegan

Background and aims: Hakea prostrata (Proteaceae) is a highly phosphorus-use-efficient plant native to southwest Australia. It maintains a high photosynthetic rate at low leaf phosphorus (P) and exhibits delayed leaf greening, a convergent adaptation that increases nutrient-use efficiency. This study aimed to provide broad physiological and gene expression profiles across leaf development, uncovering pathways leading from young leaves as nutrient sinks to mature leaves as low-nutrient, energy-transducing sources. Methods: To explore gene expression underlying delayed greening, we analysed a de novo transcriptome for H. prostrata across five stages of leaf development. Photosynthesis and respiration rates, and foliar pigment, P and nitrogen (N) concentrations were determined, including the division of P into five biochemical fractions. Key results: Transcripts encoding functions associated with leaf structure generally decreased in abundance across leaf development, concomitant with decreases in foliar concentrations of 85% for anthocyanins, 90% for P and 70% for N. The expression of genes associated with photosynthetic function increased during or after leaf expansion, in parallel with increases in photosynthetic pigments and activity, much later in leaf development than in species that do not have delayed greening. As leaves developed, transcript abundance for cytosolic and mitochondrial ribosomal proteins generally declined, whilst transcripts for chloroplast ribosomal proteins increased. Conclusions: There was a much longer temporal separation of leaf cell growth from chloroplast development in H. prostrata than is found in species that lack delayed greening. Transcriptome-guided analysis of leaf development in H. prostrata provided insight into delayed greening as a nutrient-saving strategy in severely phosphorus-impoverished landscapes.

Funding

This research was funded by grants from the Australian Research Council to H.L. and P.M.F. (DP200101013, LP0776252) and to H.L., P.M.F. and M.D. (DP140100148), University of Western Australia (UWA) Research Training Fund Fee Offset awards to T.B. and B.N., a UWA Research Training Fund Stipend award to T.B., a UWA Co-funded Postgraduate award to B.N., a Kwongan Foundation Top-up award to T.B. and a UWA Fay Gale Travel Fellowship to R.J. M.D. acknowledges grant support from NSF-IOS-EDGE-1923589, NSF-IOS-2014300, and DOE-BER-DE-SC0020358 to support MD and GW during this work.

History

Publication Date

2024-03-01

Journal

Plant and Soil

Volume

496

Pagination

24p. (p. 7-30)

Publisher

Springer Nature

ISSN

0032-079X

Rights Statement

© The Author(s) 2023 This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.