SAGA1 and SAGA2 promote starch formation around proto-pyrenoids in Arabidopsis chloroplasts.

SAGA1 and SAGA2 promote starch formation around proto-pyrenoids in Arabidopsis chloroplasts.
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DOI:
10.1073/pnas.2311013121
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发表时间:
2024-01-23
影响因子:
11.1
通讯作者:
McCormick, Alistair J.
McCormick, Alistair J.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Atkinson, Nicky;Stringer, Rhea;Mitchell, Stephen R.;Seung, David;McCormick, Alistair J.

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在陆地植物中设计基于蛋白核的CO2浓缩机制(pCCM)可以提高作物产量潜力和对气候波动的适应能力。模型预测,一个有效的pCCM需要一个障碍周围的蛋白核限制CO2扩散远离Rubisco。在许多物种中,包括模式藻类衣原体,这种屏障由淀粉板鞘组成。在这里,我们已经在拟南芥的原蛋白核周围工程淀粉板状颗粒。这项工作代表了在植物中实现功能性pCCM的关键一步,可以改善粮食安全问题。类核蛋白是一种叶绿体微区室,其中大多数藻类和一些陆生植物浓缩初级羧化酶Rubisco(核酮糖-1,5-二磷酸羧化酶/加氧酶),作为提高CO2捕获效率的CO2浓缩机制的一部分。将基于蛋白核的CO2浓缩机制(pCCM)工程化到C3作物植物中是提高产量能力和对气候变化的适应性的有希望的策略。许多类蛋白核的特征在于淀粉片鞘,其被提议作为限制CO2扩散的屏障。最近,我们已经在模式C3植物拟南芥中使用来自具有最充分研究的蛋白核的拟南芥的蛋白质重建了相分离的“原蛋白核”Rubisco基质。阿特金森,Y.毛氏K. X. Chan,A. J. McCormick,Nat. Commun. 11,6303(2020)]。在这里,我们描述了引入衣原体蛋白质StArch颗粒异常1(SAGA 1)和SAGA 2的影响,这与蛋白核淀粉生物发生和形态的调节有关。我们发现,SAGA 1定位于原蛋白核在工程拟南芥植物,这导致在形成非典型的球形淀粉颗粒封闭在原蛋白核凝聚物和相邻的板状颗粒,部分覆盖的凝聚物,但不修改叶绿体淀粉的总量累计。SAGA 2的额外表达进一步增加了淀粉合成为完全包围原蛋白核的相邻板状颗粒的比例。我们的研究结果铺平了道路,组装扩散屏障的一部分,在维管植物中的功能pCCM,同时也推进了我们的理解的作用,SAGA 1和SAGA 2淀粉鞘的形成和拓宽工程淀粉形态的途径。
Engineering a pyrenoid-based CO2 concentrating mechanism (pCCM) into land plants could improve crop yield potential and resilience to fluctuating climates. Modeling predicts that an efficient pCCM requires a barrier around the pyrenoid to limit CO2 diffusion away from Rubisco. In many species, including the model algae Chlamydomonas, this barrier consists of a sheath of starch plates. Here, we have engineered starch plate-like granules around the proto-pyrenoid in Arabidopsis. This work represents a critical step forward toward achieving a functional pCCM in plants that could ameliorate food security concerns. The pyrenoid is a chloroplastic microcompartment in which most algae and some terrestrial plants condense the primary carboxylase, Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) as part of a CO2-concentrating mechanism that improves the efficiency of CO2 capture. Engineering a pyrenoid-based CO2-concentrating mechanism (pCCM) into C3 crop plants is a promising strategy to enhance yield capacities and resilience to the changing climate. Many pyrenoids are characterized by a sheath of starch plates that is proposed to act as a barrier to limit CO2 diffusion. Recently, we have reconstituted a phase-separated “proto-pyrenoid” Rubisco matrix in the model C3 plant Arabidopsis thaliana using proteins from the alga with the most well-studied pyrenoid, Chlamydomonas reinhardtii [N. Atkinson, Y. Mao, K. X. Chan, A. J. McCormick, Nat. Commun. 11, 6303 (2020)]. Here, we describe the impact of introducing the Chlamydomonas proteins StArch Granules Abnormal 1 (SAGA1) and SAGA2, which are associated with the regulation of pyrenoid starch biogenesis and morphology. We show that SAGA1 localizes to the proto-pyrenoid in engineered Arabidopsis plants, which results in the formation of atypical spherical starch granules enclosed within the proto-pyrenoid condensate and adjacent plate-like granules that partially cover the condensate, but without modifying the total amount of chloroplastic starch accrued. Additional expression of SAGA2 further increases the proportion of starch synthesized as adjacent plate-like granules that fully encircle the proto-pyrenoid. Our findings pave the way to assembling a diffusion barrier as part of a functional pCCM in vascular plants, while also advancing our understanding of the roles of SAGA1 and SAGA2 in starch sheath formation and broadening the avenues for engineering starch morphology.
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